Pub Date : 2024-12-17Epub Date: 2024-11-25DOI: 10.1128/msystems.01427-24
Amandeep Kaur, Gerald V Minsavage, Neha Potnis, Jeffrey B Jones, Erica M Goss
The widespread use of antimicrobials that target bacterial pathogens has driven evolution of resistance, compromising the efficacy of these bactericides. Understanding the emergence and spread of resistance genes via mobile genetic elements is crucial for combating antimicrobial resistance. Copper resistance (CuR) in Xanthomonas euvesicatoria pv. perforans has severely affected the efficacy of copper-based bactericides for controlling bacterial leaf spot disease of tomato and pepper. Here, we investigated the evolutionary pathways of CuR acquisition and dissemination in X. euvesicatoria pv. perforans using an extensive collection of strains. We determined that chromosomally encoded CuR predominates over plasmid-borne CuR in multiple distinct phylogenetic groups of X. euvesicatoria pv. perforans. Our analysis revealed a single site of chromosomal integration by a CuR genomic island, although the genomic island showed sequence variation among phylogenetic groups. While chromosomal CuR was more prevalent, strains with plasmid-borne resistance conferred greater copper tolerance. Additionally, we identified strains carrying two copies of CuR genes, on plasmid and chromosome, that exhibited increased copper tolerance. Strains of X. euvesicatoria pv. perforans from the USA shared identical CuR gene sequences whether on plasmids or chromosome while different alleles were found in strains from other countries. In contrast to X. euvesicatoria pv. perforans, plasmid-borne CuR predominated in closely related pathovar, X. euvesicatoria pv. euvesicatoria. Overall, these findings contribute to a better understanding of the evolution and persistence of CuR in X. euvesicatoria pv. perforans and its closest relatives.IMPORTANCEThe emergence of antimicrobial resistance is a significant threat to agricultural production as it reduces the efficacy of various antimicrobials including copper-based bactericides that are widely used to control plant diseases. The challenge of increasing antimicrobial resistance entering a production system necessitates a deeper understanding of the dynamics and mechanisms by which pathogens acquire resistance. As a result of this research, we have identified different mechanisms of copper resistance acquisition as well as levels of copper resistance in a devastating plant pathogen, X. euvesicatoria pv. perforans. The evolution and dissemination of copper resistance in strains through plasmid or chromosomally integrated genomic island or both presents barriers to current management approaches, where growers rely heavily on copper-based bactericides to manage disease outbreaks. This knowledge is crucial when considering the continued use of existing antimicrobials or adopting alternative antimicrobials in efforts to implement enhanced antimicrobial stewardship strategies in agriculture.
针对细菌病原体的抗菌剂的广泛使用推动了抗药性的进化,损害了这些杀菌剂的功效。了解抗性基因通过移动遗传因子产生和传播的过程,对于对抗抗菌素抗药性至关重要。Xanthomonas euvesicatoria pv. perforans的铜抗性(CuR)严重影响了铜基杀菌剂控制番茄和辣椒细菌性叶斑病的效果。在这里,我们利用广泛收集的菌株研究了 X. euvesicatoria pv. perforans 中 CuR 获取和传播的进化途径。我们确定,在 X. euvesicatoria pv. perforans 的多个不同系统发生群中,染色体编码的 CuR 比质粒携带的 CuR 占优势。我们的分析揭示了一个由 CuR 基因组岛组成的染色体整合位点,尽管该基因组岛在不同系统发育群之间存在序列差异。虽然染色体 CuR 更为普遍,但具有质粒抗性的菌株耐铜性更强。此外,我们还发现质粒和染色体上携带两个 CuR 基因拷贝的菌株具有更强的耐铜性。美国的 X. euvesicatoria pv. perforans 菌株无论是质粒还是染色体上的 CuR 基因序列都完全相同,而其他国家的菌株则有不同的等位基因。与 X. euvesicatoria pv. perforans 相反,质粒携带的 CuR 在密切相关的病原菌 X. euvesicatoria pv. euvesicatoria 中占主导地位。总体而言,这些发现有助于更好地了解 CuR 在 X. euvesicatoria pv. perforans 及其近亲中的进化和持久性。重要意义抗菌素抗药性的出现对农业生产构成重大威胁,因为它会降低各种抗菌素的效力,包括广泛用于控制植物病害的铜基杀菌剂。面对生产系统中抗菌素抗药性不断增加的挑战,有必要深入了解病原体获得抗药性的动态和机制。通过这项研究,我们确定了一种毁灭性植物病原体 X. euvesicatoria pv. perforans 的不同铜抗性获取机制以及铜抗性水平。铜抗性通过质粒或染色体整合基因组岛或两者在菌株中的进化和传播,给目前的管理方法带来了障碍,种植者严重依赖铜基杀菌剂来控制病害爆发。在考虑继续使用现有抗菌剂或采用替代抗菌剂以加强农业抗菌剂管理战略时,这方面的知识至关重要。
{"title":"Evolution of copper resistance in <i>Xanthomonas euvesicatoria</i> pv. <i>perforans</i> population.","authors":"Amandeep Kaur, Gerald V Minsavage, Neha Potnis, Jeffrey B Jones, Erica M Goss","doi":"10.1128/msystems.01427-24","DOIUrl":"10.1128/msystems.01427-24","url":null,"abstract":"<p><p>The widespread use of antimicrobials that target bacterial pathogens has driven evolution of resistance, compromising the efficacy of these bactericides. Understanding the emergence and spread of resistance genes via mobile genetic elements is crucial for combating antimicrobial resistance. Copper resistance (CuR) in <i>Xanthomonas euvesicatoria</i> pv. <i>perforans</i> has severely affected the efficacy of copper-based bactericides for controlling bacterial leaf spot disease of tomato and pepper. Here, we investigated the evolutionary pathways of CuR acquisition and dissemination in <i>X. euvesicatoria</i> pv. <i>perforans</i> using an extensive collection of strains. We determined that chromosomally encoded CuR predominates over plasmid-borne CuR in multiple distinct phylogenetic groups of <i>X. euvesicatoria</i> pv. <i>perforans</i>. Our analysis revealed a single site of chromosomal integration by a CuR genomic island, although the genomic island showed sequence variation among phylogenetic groups. While chromosomal CuR was more prevalent, strains with plasmid-borne resistance conferred greater copper tolerance. Additionally, we identified strains carrying two copies of CuR genes, on plasmid and chromosome, that exhibited increased copper tolerance. Strains of <i>X. euvesicatoria</i> pv. <i>perforans</i> from the USA shared identical CuR gene sequences whether on plasmids or chromosome while different alleles were found in strains from other countries. In contrast to <i>X. euvesicatoria</i> pv. <i>perforans</i>, plasmid-borne CuR predominated in closely related pathovar, <i>X. euvesicatoria</i> pv. <i>euvesicatoria</i>. Overall, these findings contribute to a better understanding of the evolution and persistence of CuR in <i>X. euvesicatoria</i> pv. <i>perforans</i> and its closest relatives.IMPORTANCEThe emergence of antimicrobial resistance is a significant threat to agricultural production as it reduces the efficacy of various antimicrobials including copper-based bactericides that are widely used to control plant diseases. The challenge of increasing antimicrobial resistance entering a production system necessitates a deeper understanding of the dynamics and mechanisms by which pathogens acquire resistance. As a result of this research, we have identified different mechanisms of copper resistance acquisition as well as levels of copper resistance in a devastating plant pathogen, <i>X. euvesicatoria</i> pv. <i>perforans</i>. The evolution and dissemination of copper resistance in strains through plasmid or chromosomally integrated genomic island or both presents barriers to current management approaches, where growers rely heavily on copper-based bactericides to manage disease outbreaks. This knowledge is crucial when considering the continued use of existing antimicrobials or adopting alternative antimicrobials in efforts to implement enhanced antimicrobial stewardship strategies in agriculture.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0142724"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651105/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142710487","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Carbapenem-resistant hypervirulent Klebsiella pneumoniae (CR-hvKP) strains present a significant global public health threat due to their high mortality rates. This study investigated the genomic characteristics of seven ST11-K1 CR-hvKP isolates harboring highly homologous KPC-2-encoding multidrug-resistance plasmids. The strains were isolated from a Chinese tertiary hospital between 2017 and 2020. Whole-genome sequencing and bioinformatic analysis revealed various antibiotic resistance genes (ARGs) and virulence determinants. The blaKPC-2-bearing plasmids that contain multiple antibiotic-resistance genes were also identified in these strains. ISfinder and Orifinder were applied to identify insertion sequences (IS) and conjugation-related factors among these blaKPC-2-bearing plasmids. The blaKPC-2 was highly consistent in seven blaKPC-2-bearing plasmids (ISKpn6-blaKPC-2-ISKpn27-ISYps3-IS26). In addition, we found a region composed of ISIR, Tn5393, and IS26. It was located upstream of the blaCTX-M-15 gene and presented in six blaKPC-2-bearing plasmids, with pCR-hvKP221-KPC-P3 as an exception. Conjugation experiments demonstrated the horizontal transfer of resistance plasmids pCR-hvKP128-KPC-P1 and pCR-hvKP132-KPC-P1 across species. Notably, pLVPK-like virulence plasmids carrying virulence gene clusters pCR-hvKP173-Vir-P1, and pCR-hvKP221-Vir-P1 were also detected. A fusional plasmid pCR-hvKP221-Vir-P2, which carries virulence gene clusters and ARGs, was also identified. Five CR-hvKP strains displayed enhanced biofilm formation and high virulence in vivo infection models. Phylogenetic and single nucleotide polymorphism (SNP) analyses indicated a close genetic relationship among the isolates, suggesting a subclade. These findings highlight the complex genetic profiles and potential transmission mechanisms of CR-hvKP strains.
Importance: We reported seven CR-hvKP strains all carried a highly homologous blaKPC-2 integrated IncFⅡ-resistant plasmid, and two strains harbored virulence plasmids. Conjugation experiments confirmed the transferability of these plasmids, indicating a potential for resistance spread. Phylogenetic analysis clarified the relationship among the CR-hvKP isolates. This study provides insights into the phenotypic and genomic characteristics of seven ST11-K1 CR-hvKP strains. The high prevalence and potential for local outbreaks emphasize the need for effective control measures.
{"title":"Phenotypic and genomic characterization of ST11-K1 CR-hvKP with highly homologous <i>bla</i><sub>KPC-2</sub>-bearing plasmids in China.","authors":"Yu-Ling Han, Hua Wang, Hong-Zhe Zhu, Ying-Ying Lv, Wen Zhao, Yan-Yan Wang, Jian-Xun Wen, Zhi-De Hu, Jun-Rui Wang, Wen-Qi Zheng","doi":"10.1128/msystems.01101-24","DOIUrl":"10.1128/msystems.01101-24","url":null,"abstract":"<p><p>Carbapenem-resistant hypervirulent <i>Klebsiella pneumoniae</i> (CR-hvKP) strains present a significant global public health threat due to their high mortality rates. This study investigated the genomic characteristics of seven ST11-K1 CR-hvKP isolates harboring highly homologous KPC-2-encoding multidrug-resistance plasmids. The strains were isolated from a Chinese tertiary hospital between 2017 and 2020. Whole-genome sequencing and bioinformatic analysis revealed various antibiotic resistance genes (ARGs) and virulence determinants. The <i>bla</i><sub>KPC-2</sub>-bearing plasmids that contain multiple antibiotic-resistance genes were also identified in these strains. ISfinder and Orifinder were applied to identify insertion sequences (IS) and conjugation-related factors among these <i>bla</i><sub>KPC-2</sub>-bearing plasmids. The <i>bla</i><sub>KPC-2</sub> was highly consistent in seven <i>bla</i><sub>KPC-2</sub>-bearing plasmids (IS<i>Kpn6-bla</i><sub>KPC-2</sub>-IS<i>Kpn27</i>-IS<i>Yps3</i>-IS<i>26</i>). In addition, we found a region composed of IS<i>IR</i>, Tn<i>5393</i>, and IS<i>26</i>. It was located upstream of the <i>bla</i><sub>CTX-M-15</sub> gene and presented in six <i>bla</i><sub>KPC-2</sub>-bearing plasmids, with pCR-hvKP221-KPC-P3 as an exception. Conjugation experiments demonstrated the horizontal transfer of resistance plasmids pCR-hvKP128-KPC-P1 and pCR-hvKP132-KPC-P1 across species. Notably, pLVPK-like virulence plasmids carrying virulence gene clusters pCR-hvKP173-Vir-P1, and pCR-hvKP221-Vir-P1 were also detected. A fusional plasmid pCR-hvKP221-Vir-P2, which carries virulence gene clusters and ARGs, was also identified. Five CR-hvKP strains displayed enhanced biofilm formation and high virulence <i>in vivo</i> infection models. Phylogenetic and single nucleotide polymorphism (SNP) analyses indicated a close genetic relationship among the isolates, suggesting a subclade. These findings highlight the complex genetic profiles and potential transmission mechanisms of CR-hvKP strains.</p><p><strong>Importance: </strong>We reported seven CR-hvKP strains all carried a highly homologous <i>bla</i><sub>KPC-2</sub> integrated IncFⅡ-resistant plasmid, and two strains harbored virulence plasmids. Conjugation experiments confirmed the transferability of these plasmids, indicating a potential for resistance spread. Phylogenetic analysis clarified the relationship among the CR-hvKP isolates. This study provides insights into the phenotypic and genomic characteristics of seven ST11-K1 CR-hvKP strains. The high prevalence and potential for local outbreaks emphasize the need for effective control measures.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0110124"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651102/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142648311","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-07DOI: 10.1128/msystems.01132-24
Tommy H Tran, Isabel F Escapa, Ari Q Roberts, Wei Gao, Abiola C Obawemimo, Julia A Segre, Heidi H Kong, Sean Conlan, Matthew S Kelly, Katherine P Lemon
<p><p><i>Corynebact</i>e<i>rium</i> species are globally ubiquitous in human nasal microbiota across the lifespan. Moreover, nasal microbiota profiles typified by higher relative abundances of <i>Corynebacterium</i> are often positively associated with health. Among the most common human nasal <i>Corynebacterium</i> species are <i>C. propinquum</i>, <i>C. pseudodiphtheriticum, C. accolens</i>, and <i>C. tuberculostearicum</i>. To gain insight into the functions of these four species, we identified genomic, phylogenomic, and pangenomic properties and estimated the metabolic capabilities of 87 distinct human nasal <i>Corynebacterium</i> strain genomes: 31 from Botswana and 56 from the United States. <i>C. pseudodiphtheriticum</i> had geographically distinct clades consistent with localized strain circulation, whereas some strains from the other species had wide geographic distribution spanning Africa and North America. All species had similar genomic and pangenomic structures. Gene clusters assigned to all COG metabolic categories were overrepresented in the persistent versus accessory genome of each species indicating limited strain-level variability in metabolic capacity. Based on prevalence data, at least two <i>Corynebacterium</i> species likely coexist in the nasal microbiota of 82% of adults. So, it was surprising that core metabolic capabilities were highly conserved among the four species indicating limited species-level metabolic variation. Strikingly, strains in the U.S. clade of <i>C. pseudodiphtheriticum</i> lacked genes for assimilatory sulfate reduction present in most of the strains in the Botswana clade and in the other studied species, indicating a recent, geographically related loss of assimilatory sulfate reduction. Overall, the minimal species and strain variability in metabolic capacity implies coexisting strains might have limited ability to occupy distinct metabolic niches.</p><p><strong>Importance: </strong>Pangenomic analysis with estimation of functional capabilities facilitates our understanding of the full biologic diversity of bacterial species. We performed systematic genomic, phylogenomic, and pangenomic analyses with qualitative estimation of the metabolic capabilities of four common human nasal <i>Corynebacterium</i> species, along with focused experimental validations, generating a foundational resource. The prevalence of each species in human nasal microbiota is consistent with the common coexistence of at least two species. We identified a notably high level of metabolic conservation within and among species indicating limited options for species to occupy distinct metabolic niches, highlighting the importance of investigating interactions among nasal <i>Corynebacterium</i> species. Comparing strains from two continents, <i>C. pseudodiphtheriticum</i> had restricted geographic strain distribution characterized by an evolutionarily recent loss of assimilatory sulfate reduction in U.S. strains. Our findings contrib
在人的一生中,棒状杆菌在鼻腔微生物群中无处不在。此外,鼻腔微生物区系中相对丰度较高的棒状杆菌往往与健康呈正相关。人类鼻腔中最常见的棒状杆菌种类包括 C. propinquum、C. pseudodiphtheriticum、C. accolens 和 C. tuberculostearicum。为了深入了解这四个物种的功能,我们确定了基因组、系统基因组和泛基因组的特性,并估算了 87 个不同人类鼻腔棒状杆菌菌株基因组的代谢能力:其中 31 株来自博茨瓦纳,56 株来自美国。伪双歧杆菌具有与本地菌株循环相一致的不同地理支系,而其他物种的一些菌株则具有跨越非洲和北美的广泛地理分布。所有物种的基因组和泛基因组结构相似。分配给所有 COG 代谢类别的基因簇在每个物种的持久基因组和附属基因组中都有较高的代表性,这表明菌株代谢能力的变异性有限。根据流行率数据,82% 的成年人的鼻腔微生物群中可能至少有两种科里纳菌共存。因此,令人惊讶的是,这四个物种的核心代谢能力高度一致,表明物种水平的代谢变异有限。令人吃惊的是,美国支系的假嗜血杆菌菌株缺乏硫酸盐同化还原基因,而博茨瓦纳支系和其他研究物种的大多数菌株中都有这种基因,这表明硫酸盐同化还原基因的丧失与最近的地理位置有关。总体而言,物种和菌株在代谢能力方面的差异极小,这意味着共存菌株占据不同代谢位点的能力可能有限:重要意义:通过估算功能能力进行庞基因组分析有助于我们了解细菌物种的全部生物多样性。我们进行了系统的基因组学、系统发生组学和庞基因组学分析,对四种常见的人类鼻腔棒状杆菌的代谢能力进行了定性估计,并进行了重点实验验证,从而生成了一种基础资源。每个物种在人类鼻腔微生物群中的流行程度与至少两个物种共存的情况一致。我们在物种内部和物种之间发现了明显的高水平代谢保护,这表明物种占据不同代谢壁龛的选择有限,突出了研究鼻腔棒状杆菌物种之间相互作用的重要性。通过比较来自两大洲的菌株,假双歧杆菌的地理菌株分布受到限制,其特点是美国菌株在进化过程中丧失了同化硫酸盐还原的能力。我们的研究结果有助于了解假丝酵母菌在人类鼻腔微生物群中的功能,并评估其未来用作生物治疗的潜力。
{"title":"Metabolic capabilities are highly conserved among human nasal-associated <i>Corynebacterium</i> species in pangenomic analyses.","authors":"Tommy H Tran, Isabel F Escapa, Ari Q Roberts, Wei Gao, Abiola C Obawemimo, Julia A Segre, Heidi H Kong, Sean Conlan, Matthew S Kelly, Katherine P Lemon","doi":"10.1128/msystems.01132-24","DOIUrl":"10.1128/msystems.01132-24","url":null,"abstract":"<p><p><i>Corynebact</i>e<i>rium</i> species are globally ubiquitous in human nasal microbiota across the lifespan. Moreover, nasal microbiota profiles typified by higher relative abundances of <i>Corynebacterium</i> are often positively associated with health. Among the most common human nasal <i>Corynebacterium</i> species are <i>C. propinquum</i>, <i>C. pseudodiphtheriticum, C. accolens</i>, and <i>C. tuberculostearicum</i>. To gain insight into the functions of these four species, we identified genomic, phylogenomic, and pangenomic properties and estimated the metabolic capabilities of 87 distinct human nasal <i>Corynebacterium</i> strain genomes: 31 from Botswana and 56 from the United States. <i>C. pseudodiphtheriticum</i> had geographically distinct clades consistent with localized strain circulation, whereas some strains from the other species had wide geographic distribution spanning Africa and North America. All species had similar genomic and pangenomic structures. Gene clusters assigned to all COG metabolic categories were overrepresented in the persistent versus accessory genome of each species indicating limited strain-level variability in metabolic capacity. Based on prevalence data, at least two <i>Corynebacterium</i> species likely coexist in the nasal microbiota of 82% of adults. So, it was surprising that core metabolic capabilities were highly conserved among the four species indicating limited species-level metabolic variation. Strikingly, strains in the U.S. clade of <i>C. pseudodiphtheriticum</i> lacked genes for assimilatory sulfate reduction present in most of the strains in the Botswana clade and in the other studied species, indicating a recent, geographically related loss of assimilatory sulfate reduction. Overall, the minimal species and strain variability in metabolic capacity implies coexisting strains might have limited ability to occupy distinct metabolic niches.</p><p><strong>Importance: </strong>Pangenomic analysis with estimation of functional capabilities facilitates our understanding of the full biologic diversity of bacterial species. We performed systematic genomic, phylogenomic, and pangenomic analyses with qualitative estimation of the metabolic capabilities of four common human nasal <i>Corynebacterium</i> species, along with focused experimental validations, generating a foundational resource. The prevalence of each species in human nasal microbiota is consistent with the common coexistence of at least two species. We identified a notably high level of metabolic conservation within and among species indicating limited options for species to occupy distinct metabolic niches, highlighting the importance of investigating interactions among nasal <i>Corynebacterium</i> species. Comparing strains from two continents, <i>C. pseudodiphtheriticum</i> had restricted geographic strain distribution characterized by an evolutionarily recent loss of assimilatory sulfate reduction in U.S. strains. Our findings contrib","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0113224"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651106/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142604711","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-18DOI: 10.1128/msystems.01403-24
Angel Rain-Franco, Alizée Le Moigne, Lucas Serra Moncadas, Marisa O D Silva, Adrian-Stefan Andrei, Jakob Pernthaler
Segregation and mixing shape the structure and functioning of aquatic microbial communities, but their respective roles are challenging to disentangle in field studies. We explored the hypothesis that functional differences and beta diversity among stochastically assembled communities would increase in the absence of dispersal. Contrariwise, we expected biotic selection during homogenizing dispersal to reduce beta and gamma diversity as well as functional variability. This was experimentally addressed by examining the compositional and functional changes of 20 freshwater bacterial assemblages maintained at identical conditions over seven growth cycles for 34 days and subjected to two consecutive dispersal regimes. Initial dispersal limitation generated high beta diversity and led to the repeated emergence of community types that were dominated by particular taxa. Compositional stability and evenness of the community types varied over successive growth cycles, reflecting differences in functional properties. Carbon use efficiency increased during cultivation, with some communities of unique composition outperforming the replicate community types. Homogenizing dispersal led to high compositional similarity and reduced gamma diversity. While a neutral and a competition-based (Elo-rating) model together largely explained community assembly, a pseudomonad disproportionally dominated across communities, possibly due to interaction-related genomic traits. In conclusion, microbial assemblages stochastically generated by dispersal limitation can be gradually "refined" into distinct community types by subsequent deterministic processes. Segregation of communities represented an insurance mechanism for highly productive but competitively weak microbial taxa that were excluded during community coalescence.
Importance: We experimentally assessed the compositional and functional responses of freshwater bacterial assemblages exposed to two consecutive dispersal-related events (dispersal limitation and homogenizing dispersal) under identical growth conditions. While segregation led to a decreased local diversity, high beta diversity sustained regional diversity and functional variability. In contrast, homogenizing dispersal reduced the species pool and functional variability of the metacommunity. Our findings highlight the role of dispersal in regulating both diversity and functional variability of aquatic microbial metacommunities, thereby providing crucial insight to predict changes in ecosystem functioning.
{"title":"Dispersal shapes compositional and functional diversity in aquatic microbial communities.","authors":"Angel Rain-Franco, Alizée Le Moigne, Lucas Serra Moncadas, Marisa O D Silva, Adrian-Stefan Andrei, Jakob Pernthaler","doi":"10.1128/msystems.01403-24","DOIUrl":"10.1128/msystems.01403-24","url":null,"abstract":"<p><p>Segregation and mixing shape the structure and functioning of aquatic microbial communities, but their respective roles are challenging to disentangle in field studies. We explored the hypothesis that functional differences and beta diversity among stochastically assembled communities would increase in the absence of dispersal. Contrariwise, we expected biotic selection during homogenizing dispersal to reduce beta and gamma diversity as well as functional variability. This was experimentally addressed by examining the compositional and functional changes of 20 freshwater bacterial assemblages maintained at identical conditions over seven growth cycles for 34 days and subjected to two consecutive dispersal regimes. Initial dispersal limitation generated high beta diversity and led to the repeated emergence of community types that were dominated by particular taxa. Compositional stability and evenness of the community types varied over successive growth cycles, reflecting differences in functional properties. Carbon use efficiency increased during cultivation, with some communities of unique composition outperforming the replicate community types. Homogenizing dispersal led to high compositional similarity and reduced gamma diversity. While a neutral and a competition-based (Elo-rating) model together largely explained community assembly, a pseudomonad disproportionally dominated across communities, possibly due to interaction-related genomic traits. In conclusion, microbial assemblages stochastically generated by dispersal limitation can be gradually \"refined\" into distinct community types by subsequent deterministic processes. Segregation of communities represented an insurance mechanism for highly productive but competitively weak microbial taxa that were excluded during community coalescence.</p><p><strong>Importance: </strong>We experimentally assessed the compositional and functional responses of freshwater bacterial assemblages exposed to two consecutive dispersal-related events (dispersal limitation and homogenizing dispersal) under identical growth conditions. While segregation led to a decreased local diversity, high beta diversity sustained regional diversity and functional variability. In contrast, homogenizing dispersal reduced the species pool and functional variability of the metacommunity. Our findings highlight the role of dispersal in regulating both diversity and functional variability of aquatic microbial metacommunities, thereby providing crucial insight to predict changes in ecosystem functioning.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0140324"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651098/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142648308","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-21DOI: 10.1128/msystems.01345-24
Jian Huang, Yanzhuan Lu, Fengwei Tian, Yongqing Ni
The exponential growth of high-throughput sequencing (HTS) data on the microbial communities presents researchers with an unparalleled opportunity to delve deeper into the association of microorganisms with host phenotype. However, this growth also poses a challenge, as microbial data are complex, sparse, discrete, and prone to zero inflation. Herein, by utilizing 10 distinct counting models for analyzing simulated data, we proposed an innovative Bayesian zero-inflated negative binomial (ZINB) regression model that is capable of identifying differentially abundant taxa associated with distinctive host phenotypes and quantifying the effects of covariates on these taxa. Our proposed model exhibits excellent accuracy compared with conventional Hurdle and INLA models, especially in scenarios characterized by inflation and overdispersion. Moreover, we confirm that dispersion parameters significantly affect the accuracy of model results, with defects gradually alleviating as the number of analyzed samples increases. Subsequently applying our model to amplicon data in real multi-ethnic children cohort, we found that only a subset of taxa were identified as having zero inflation in real data, suggesting that the prevailing understanding and processing of microbial count data in most previous microbiome studies were overly dogmatic. In practice, our pipeline of integrating bacterial differential abundance in microbiome data and relevant covariates is effective and feasible. Taken together, our method is expected to be extended to the microbiota studies of various multi-cohort populations.
Importance: The microbiome is closely associated with physical indicators of the body, such as height, weight, age and BMI, which can be used as measures of human health. Accurately identifying which taxa in the microbiome are closely related to indicators of physical development is valuable as microbial markers of regional child growth trajectory. Zero-inflated negative binomial (ZINB) model, a type of Bayesian generalized linear model, can be effectively modeled in complex biological systems. We present an innovative ZINB regression model that is capable of identifying differentially abundant taxa associated with distinctive host phenotypes and quantifying the effects of covariates on these taxa, and demonstrate that its accuracy is superior to traditional Hurdle and INLA models. Our pipeline of integrating bacterial differential abundance in microbiome data and relevant covariates is effective and feasible.
{"title":"Association of body index with fecal microbiome in children cohorts with ethnic-geographic factor interaction: accurately using a Bayesian zero-inflated negative binomial regression model.","authors":"Jian Huang, Yanzhuan Lu, Fengwei Tian, Yongqing Ni","doi":"10.1128/msystems.01345-24","DOIUrl":"10.1128/msystems.01345-24","url":null,"abstract":"<p><p>The exponential growth of high-throughput sequencing (HTS) data on the microbial communities presents researchers with an unparalleled opportunity to delve deeper into the association of microorganisms with host phenotype. However, this growth also poses a challenge, as microbial data are complex, sparse, discrete, and prone to zero inflation. Herein, by utilizing 10 distinct counting models for analyzing simulated data, we proposed an innovative Bayesian zero-inflated negative binomial (ZINB) regression model that is capable of identifying differentially abundant taxa associated with distinctive host phenotypes and quantifying the effects of covariates on these taxa. Our proposed model exhibits excellent accuracy compared with conventional Hurdle and INLA models, especially in scenarios characterized by inflation and overdispersion. Moreover, we confirm that dispersion parameters significantly affect the accuracy of model results, with defects gradually alleviating as the number of analyzed samples increases. Subsequently applying our model to amplicon data in real multi-ethnic children cohort, we found that only a subset of taxa were identified as having zero inflation in real data, suggesting that the prevailing understanding and processing of microbial count data in most previous microbiome studies were overly dogmatic. In practice, our pipeline of integrating bacterial differential abundance in microbiome data and relevant covariates is effective and feasible. Taken together, our method is expected to be extended to the microbiota studies of various multi-cohort populations.</p><p><strong>Importance: </strong>The microbiome is closely associated with physical indicators of the body, such as height, weight, age and BMI, which can be used as measures of human health. Accurately identifying which taxa in the microbiome are closely related to indicators of physical development is valuable as microbial markers of regional child growth trajectory. Zero-inflated negative binomial (ZINB) model, a type of Bayesian generalized linear model, can be effectively modeled in complex biological systems. We present an innovative ZINB regression model that is capable of identifying differentially abundant taxa associated with distinctive host phenotypes and quantifying the effects of covariates on these taxa, and demonstrate that its accuracy is superior to traditional Hurdle and INLA models. Our pipeline of integrating bacterial differential abundance in microbiome data and relevant covariates is effective and feasible.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0134524"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651110/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142681116","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-25DOI: 10.1128/msystems.01298-24
Jessica R Bernardin, Erica B Young, Sarah M Gray, Leonora S Bittleston
Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community's functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (Sarracenia purpurea). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, including S. purpurea. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth.
Importance: This study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions.
{"title":"Bacterial community function increases leaf growth in a pitcher plant experimental system.","authors":"Jessica R Bernardin, Erica B Young, Sarah M Gray, Leonora S Bittleston","doi":"10.1128/msystems.01298-24","DOIUrl":"10.1128/msystems.01298-24","url":null,"abstract":"<p><p>Across diverse ecosystems, bacteria and their hosts engage in complex relationships having negative, neutral, or positive interactions. However, the specific effects of leaf-associated bacterial community functions on plant growth are poorly understood. Although microbes can promote plant growth through various biochemical mechanisms, investigating the community's functional contributions to plant growth remains to be explored. To address this gap, we characterized the relationships between bacterial community function and host plant growth in the purple pitcher plant (<i>Sarracenia purpurea</i>). The main aim of our research was to investigate how different bacterial community functions affect the growth and nutrient content in the plant. Previous research has suggested that microbial communities aid in prey decomposition and subsequent nutrient acquisition in carnivorous plants, including <i>S. purpurea</i>. However, the specific functional roles of bacterial communities in plant growth and nutrient uptake are not well known. In this study, sterile, freshly opened pitchers were inoculated with three functionally distinct, pre-assembled bacterial communities. Bacterial community composition and function were measured over 8 weeks using physiological assays, metagenomics, and metatranscriptomics. Distinct community functions affected plant traits; a bacterial community enriched in decomposition was associated with larger leaves with almost double the biomass of control pitchers. Physiological differences in bacterial communities were supported by metatranscriptomics; for example, the bacterial community with the highest chitinase activity had greater expression of transcripts associated with chitinase enzymes. The relationship between bacterial community function and plant growth observed here indicates potential mechanisms, such as chitinase activity, for host-associated bacterial functions to support pitcher plant growth.</p><p><strong>Importance: </strong>This study addresses a gap in understanding the relationships between bacterial community function and plant growth. We inoculated sterile, freshly opened pitcher plant leaves with three functionally distinct bacterial communities to uncover potential mechanisms through which bacterial functions support plant health and growth. Our findings demonstrate that distinct community functions significantly influence plant traits, with some bacterial communities supporting more plant growth than in control pitchers. These results highlight the ecological roles of microbial communities in plants and thus ecosystems and suggest that nutrient cycling is an important pathway through which microbes support host plant health. This research provides valuable insights into plant-microbe interactions and the effects of diverse microbial community functions.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0129824"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651108/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142710482","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-12DOI: 10.1128/msystems.00762-24
Vasni Zavaleta, Laura Pérez-Través, Luis A Saona, Carlos A Villarroel, Amparo Querol, Francisco A Cubillos
<p><p>Hybridization between <i>Saccharomyces cerevisiae</i> and <i>Saccharomyces eubayanus</i> resulted in the emergence of <i>S. pastorianus</i>, a crucial yeast for lager fermentation. However, our understanding of hybridization success and hybrid vigor between these two species remains limited due to the scarcity of <i>S. eubayanus</i> parental strains. Here, we explore hybridization success and the impact of hybridization on fermentation performance and volatile compound profiles in newly formed lager hybrids. By selecting parental candidates spanning a diverse array of lineages from both species, we reveal that the Beer and PB-2 lineages exhibit high rates of hybridization success in <i>S. cerevisiae</i> and <i>S. eubayanus</i>, respectively. Polyploid hybrids were generated through a spontaneous diploid hybridization technique (rare-mating), revealing a prevalence of triploids and diploids over tetraploids. Despite the absence of heterosis in fermentative capacity, hybrids displayed phenotypic variability, notably influenced by maltotriose consumption. Interestingly, ploidy levels did not significantly correlate with fermentative capacity, although triploids exhibited greater phenotypic variability. The <i>S. cerevisiae</i> parental lineages primarily influenced volatile compound profiles, with significant differences in aroma production. Interestingly, hybrids emerging from the Beer <i>S. cerevisiae</i> parental lineages exhibited a volatile compound profile resembling the corresponding <i>S. eubayanus</i> parent. This pattern may result from the dominant inheritance of the <i>S. eubayanus</i> aroma profile, as suggested by the over-expression of genes related to alcohol metabolism and acetate synthesis in hybrids including the Beer <i>S. cerevisiae</i> lineage. Our findings suggest complex interactions between parental lineages and hybridization outcomes, highlighting the potential for creating yeasts with distinct brewing traits through hybridization strategies.</p><p><strong>Importance: </strong>Our study investigates the principles of lager yeast hybridization between <i>Saccharomyces cerevisiae</i> and <i>Saccharomyces eubayanus</i>. This process gave rise to the lager yeast <i>Saccharomyces pastorianus</i>. By examining how these novel hybrids perform during fermentation and the aromas they produce, we uncover the genetic bases of brewing trait inheritance. We successfully generated polyploid hybrids using diverse strains and lineages from both parent species, predominantly triploids and diploids. Although these hybrids did not show improved fermentation capacity, they exhibited varied traits, especially in utilizing maltotriose, a key sugar in brewing. Remarkably, the aroma profiles of these hybrids were primarily influenced by the <i>S. cerevisiae</i> parent, with Beer lineage hybrids adopting aroma characteristics from their <i>S. eubayanus</i> parent. These insights reveal the complex genetic interactions in hybrid yeasts, openin
酿酒酵母(Saccharomyces cerevisiae)和酿酒酵母(Saccharomyces eubayanus)杂交产生了酿酒酵母(S. pastorianus),它是啤酒发酵的一种重要酵母。然而,由于 S. eubayanus 亲本菌株的稀缺,我们对这两个物种之间杂交成功率和杂交活力的了解仍然有限。在此,我们探讨了杂交成功率以及杂交对新形成的拉格杂交种的发酵性能和挥发性化合物特征的影响。通过从两个物种中选择不同品系的候选亲本,我们发现啤酒品系和 PB-2 品系分别在 S. cerevisiae 和 S. eubayanus 中表现出很高的杂交成功率。通过自发二倍体杂交技术(稀有交配)产生的多倍体杂交种显示,三倍体和二倍体比四倍体更普遍。尽管在发酵能力方面没有异交现象,但杂交种表现出了表型变异性,特别是受麦芽三糖消耗量的影响。有趣的是,虽然三倍体表现出更大的表型变异性,但倍性水平与发酵能力并无明显关联。S. cerevisiae 亲本品系主要影响挥发性化合物特征,在香气产生方面存在显著差异。有趣的是,从啤酒酿造菌(S. cerevisiae)亲本品系中产生的杂交种表现出与相应的啤酒酿造菌(S. eubayanus)亲本相似的挥发性化合物特征。这种模式可能是由 S. eubayanus 香气特征的显性遗传造成的,与酒精代谢和乙酸酯合成相关的基因在包括啤酒酿造啤酒 S. cerevisiae 品系的杂交种中过度表达也说明了这一点。我们的研究结果表明,亲本品系与杂交结果之间存在复杂的相互作用,凸显了通过杂交策略创造具有独特酿造特性的酵母菌的潜力:我们的研究调查了酿酒酵母与酿酒酵母杂交的原理。这一过程产生了酿酒酵母牧酵母。通过研究这些新型杂交种在发酵过程中的表现及其产生的香气,我们揭示了酿造性状遗传的基因基础。我们利用来自两个亲本物种的不同菌株和品系,主要是三倍体和二倍体,成功地产生了多倍体杂交种。虽然这些杂交种的发酵能力没有得到提高,但它们表现出了不同的性状,尤其是在利用麦芽三糖(酿造中的一种关键糖分)方面。值得注意的是,这些杂交种的香气特征主要受 S. cerevisiae 亲本的影响,而 Beer 系杂交种则采用了其 S. eubayanus 亲本的香气特征。这些发现揭示了杂交酵母中复杂的基因相互作用,为制造具有理想性状的独特酿酒酵母提供了新的可能性。
{"title":"Understanding brewing trait inheritance in <i>de novo</i> Lager yeast hybrids.","authors":"Vasni Zavaleta, Laura Pérez-Través, Luis A Saona, Carlos A Villarroel, Amparo Querol, Francisco A Cubillos","doi":"10.1128/msystems.00762-24","DOIUrl":"10.1128/msystems.00762-24","url":null,"abstract":"<p><p>Hybridization between <i>Saccharomyces cerevisiae</i> and <i>Saccharomyces eubayanus</i> resulted in the emergence of <i>S. pastorianus</i>, a crucial yeast for lager fermentation. However, our understanding of hybridization success and hybrid vigor between these two species remains limited due to the scarcity of <i>S. eubayanus</i> parental strains. Here, we explore hybridization success and the impact of hybridization on fermentation performance and volatile compound profiles in newly formed lager hybrids. By selecting parental candidates spanning a diverse array of lineages from both species, we reveal that the Beer and PB-2 lineages exhibit high rates of hybridization success in <i>S. cerevisiae</i> and <i>S. eubayanus</i>, respectively. Polyploid hybrids were generated through a spontaneous diploid hybridization technique (rare-mating), revealing a prevalence of triploids and diploids over tetraploids. Despite the absence of heterosis in fermentative capacity, hybrids displayed phenotypic variability, notably influenced by maltotriose consumption. Interestingly, ploidy levels did not significantly correlate with fermentative capacity, although triploids exhibited greater phenotypic variability. The <i>S. cerevisiae</i> parental lineages primarily influenced volatile compound profiles, with significant differences in aroma production. Interestingly, hybrids emerging from the Beer <i>S. cerevisiae</i> parental lineages exhibited a volatile compound profile resembling the corresponding <i>S. eubayanus</i> parent. This pattern may result from the dominant inheritance of the <i>S. eubayanus</i> aroma profile, as suggested by the over-expression of genes related to alcohol metabolism and acetate synthesis in hybrids including the Beer <i>S. cerevisiae</i> lineage. Our findings suggest complex interactions between parental lineages and hybridization outcomes, highlighting the potential for creating yeasts with distinct brewing traits through hybridization strategies.</p><p><strong>Importance: </strong>Our study investigates the principles of lager yeast hybridization between <i>Saccharomyces cerevisiae</i> and <i>Saccharomyces eubayanus</i>. This process gave rise to the lager yeast <i>Saccharomyces pastorianus</i>. By examining how these novel hybrids perform during fermentation and the aromas they produce, we uncover the genetic bases of brewing trait inheritance. We successfully generated polyploid hybrids using diverse strains and lineages from both parent species, predominantly triploids and diploids. Although these hybrids did not show improved fermentation capacity, they exhibited varied traits, especially in utilizing maltotriose, a key sugar in brewing. Remarkably, the aroma profiles of these hybrids were primarily influenced by the <i>S. cerevisiae</i> parent, with Beer lineage hybrids adopting aroma characteristics from their <i>S. eubayanus</i> parent. These insights reveal the complex genetic interactions in hybrid yeasts, openin","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0076224"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651111/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142624254","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-12DOI: 10.1128/msystems.01142-24
Ye Jin, Chenyang Gao, Gaoqin Teng, Zhenchao Zhou, Wangxiao Zhou, Man Huang
<p><p><i>Staphylococcus aureus</i> sequence type (ST) 88, encompassing both methicillin-resistant <i>S. aureus</i> (MRSA) and methicillin-sensitive <i>S. aureus</i> (MSSA) phenotypes, is globally prevalent and commonly associated with skin and soft tissue infections. Despite its widespread occurrence, comprehensive genomic studies on this clone remain scarce. In this study, we performed detailed genomic analyses on 130 ST88 isolates derived from severe bloodstream infections alongside 275 publicly available ST88 sequences. Our phylogenetic analysis identified four distinct clades, with evidence suggesting independent evolution and significant clonal expansion of ST88 in China, particularly within clade I, which appeared to have emerged circa 1964. We documented notable interregional, international, and even intercontinental transmission of ST88 isolates. Variability in the distribution of SCC<i>mec</i> and <i>spa</i> types was observed across clades. Our <i>in silico</i> analyses indicated distinct patterns in the distribution of resistance genes, virulence genes, and mobile genetic elements among the clades, with clade I notably harboring the highest prevalence of the intact <i>sraP</i> gene and an independently acquired novel prophage, φST88-1. Conversely, clade IV exhibited deletions within the <i>sasC</i> gene, with certain sub-clades lacking the <i>sdrDE</i> and <i>fnbB</i> genes, underscoring the superior adhesive capabilities of clade I. <i>In vitro</i> experiments confirmed enhanced biofilm formation in clade I isolates, although the levels of hemolysis and cytotoxicity were similar across clades. Pan-genome-wide association study revealed that core SNPs, rather than the accessory genome, are the primary contributors to the diversification of the ST88 clades. These findings enrich our understanding of the genetic foundations underpinning the transmission dynamics and phenotypic diversity of ST88 clones globally.IMPORTANCEUnderstanding the evolution and transmission of <i>Staphylococcus aureus</i> ST88 clones is critically important due to their spread within food, hospital, and community environments, leading to significant health issues. Despite its prevalence, detailed genomic insights into ST88, particularly regarding its diversity and evolutionary dynamics, have been lacking. Our comprehensive genomic analysis of 130 ST88 isolates from severe bloodstream infections, alongside 275 sequences from public databases, significantly advances our understanding of this pathogen. We identified four distinct evolutionary clades, demonstrating the independent evolution and substantial clonal expansion of ST88 in China, as well as its ability to spread across regions and continents. The diversity among the isolates was evident in their unique profiles of <i>SCCmec</i> elements, antibiotic resistance genes, virulence genes, and mobile genetic elements. Our findings underscore the critical role of core genomic variations over accessory elements in d
{"title":"Dissecting the genetic features and evolution of <i>Staphylococcus aureus</i> sequence type 88: a global perspective.","authors":"Ye Jin, Chenyang Gao, Gaoqin Teng, Zhenchao Zhou, Wangxiao Zhou, Man Huang","doi":"10.1128/msystems.01142-24","DOIUrl":"10.1128/msystems.01142-24","url":null,"abstract":"<p><p><i>Staphylococcus aureus</i> sequence type (ST) 88, encompassing both methicillin-resistant <i>S. aureus</i> (MRSA) and methicillin-sensitive <i>S. aureus</i> (MSSA) phenotypes, is globally prevalent and commonly associated with skin and soft tissue infections. Despite its widespread occurrence, comprehensive genomic studies on this clone remain scarce. In this study, we performed detailed genomic analyses on 130 ST88 isolates derived from severe bloodstream infections alongside 275 publicly available ST88 sequences. Our phylogenetic analysis identified four distinct clades, with evidence suggesting independent evolution and significant clonal expansion of ST88 in China, particularly within clade I, which appeared to have emerged circa 1964. We documented notable interregional, international, and even intercontinental transmission of ST88 isolates. Variability in the distribution of SCC<i>mec</i> and <i>spa</i> types was observed across clades. Our <i>in silico</i> analyses indicated distinct patterns in the distribution of resistance genes, virulence genes, and mobile genetic elements among the clades, with clade I notably harboring the highest prevalence of the intact <i>sraP</i> gene and an independently acquired novel prophage, φST88-1. Conversely, clade IV exhibited deletions within the <i>sasC</i> gene, with certain sub-clades lacking the <i>sdrDE</i> and <i>fnbB</i> genes, underscoring the superior adhesive capabilities of clade I. <i>In vitro</i> experiments confirmed enhanced biofilm formation in clade I isolates, although the levels of hemolysis and cytotoxicity were similar across clades. Pan-genome-wide association study revealed that core SNPs, rather than the accessory genome, are the primary contributors to the diversification of the ST88 clades. These findings enrich our understanding of the genetic foundations underpinning the transmission dynamics and phenotypic diversity of ST88 clones globally.IMPORTANCEUnderstanding the evolution and transmission of <i>Staphylococcus aureus</i> ST88 clones is critically important due to their spread within food, hospital, and community environments, leading to significant health issues. Despite its prevalence, detailed genomic insights into ST88, particularly regarding its diversity and evolutionary dynamics, have been lacking. Our comprehensive genomic analysis of 130 ST88 isolates from severe bloodstream infections, alongside 275 sequences from public databases, significantly advances our understanding of this pathogen. We identified four distinct evolutionary clades, demonstrating the independent evolution and substantial clonal expansion of ST88 in China, as well as its ability to spread across regions and continents. The diversity among the isolates was evident in their unique profiles of <i>SCCmec</i> elements, antibiotic resistance genes, virulence genes, and mobile genetic elements. Our findings underscore the critical role of core genomic variations over accessory elements in d","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0114224"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651095/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142624246","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-12-17Epub Date: 2024-11-27DOI: 10.1128/msystems.00954-24
Yuanda Gao, Hangyu Zhang, Dapeng Zhu, Long Guo
Captive otters raised in zoos are fed different artificial diets, which may shape gut microbiota. The objective is to evaluate the impacts of two different artificial diets on microbial communities and function capabilities and short-chain fatty acid (SCFA) profiles in healthy otters' feces. A total of 16 Asian small-clawed otters in two groups (n = 8) were selected. Group A otters were fed raw loaches supplemented with commercial cat food (LSCF) diet, and group B otters were fed raw crucian diet. The communities and functional capabilities of microbiota in feces were assessed with metagenomic sequencing. Captive otters fed two kinds of diets possessed different gut microbial communities and functional capabilities. Various pathogenic bacteria, like Escherichia coli and Clostridium perfringens, were enriched in the samples from the two groups, respectively. Most of the differential pathways of nutrient metabolism were significantly enriched in group A, and the distributions of carbohydrate enzymes in the two groups significantly differed from each other. Multiple resistance genes markedly accumulated in fecal samples of the group A otters with LSCF diet. Higher concentrations of SCFAs were also observed in group A otters. Two feeding strategies were both likely to facilitate the colonization and expansion of various pathogenic bacteria and the accumulation of resistance genes in the intestines of captive otters, suggesting that risk of pathogen transmission existed in the current feeding process. Commercial cat food could supplement various nutrients and provide a substrate for the production of SCFAs, which might be beneficial for the otters' intestinal fermentation and metabolism.
Importance: Captive otters fed with different diets possessed distinct gut microbial communities and functions, with the enrichment of several pathogens and multiple resistance genes in their gut microbiota. The current artificial feeding strategies had the possibility to accelerate the colonization and proliferation of various pathogenic bacteria in the intestines of otters and the spread of resistance genes, increasing the risk of diseases. In addition, supplementation with commercial cat food had benefits for otters' intestinal fermentation and the metabolism of gut microbiota.
动物园饲养的人工饲养水獭喂食不同的人工饲料,这可能会影响肠道微生物群。本研究的目的是评估两种不同人工饲料对健康水獭粪便中微生物群落和功能能力以及短链脂肪酸(SCFA)特征的影响。研究人员选择了两组共 16 只亚洲小爪水獭(n = 8)。A 组水獭生喂泥鳅,辅以商品猫粮(LSCF),B 组水獭生喂鲫鱼。通过元基因组测序评估了粪便中微生物群的群落和功能。喂食两种食物的人工饲养水獭拥有不同的肠道微生物群落和功能。大肠杆菌和产气荚膜梭菌等致病菌分别在两组样本中富集。营养代谢的大多数差异途径在 A 组中明显富集,碳水化合物酶在两组中的分布也有显著差异。在以 LSCF 为食的 A 组水獭粪便样本中,多种抗性基因明显积累。在 A 组水獭中还观察到较高浓度的 SCFAs。两种喂养策略都可能促进各种病原菌在圈养水獭肠道中的定植和扩展以及抗性基因的积累,这表明目前的喂养过程中存在病原体传播的风险。商品猫粮可以补充各种营养物质,并为SCFAs的产生提供基质,这可能有利于水獭的肠道发酵和新陈代谢:用不同食物喂养的人工饲养水獭拥有不同的肠道微生物群落和功能,其肠道微生物群中富含多种病原体和多种抗性基因。目前的人工喂养策略有可能加速各种病原菌在水獭肠道中的定植和增殖以及抗性基因的传播,增加患病风险。此外,补充商品猫粮对水獭的肠道发酵和肠道微生物群的新陈代谢也有好处。
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Pub Date : 2024-12-17Epub Date: 2024-11-06DOI: 10.1128/msystems.00568-24
Wei Xiao, J L Weissman, Philip L F Johnson
CRISPR-Cas is the only known adaptive immune system of prokaryotes. It is a powerful defense system against mobile genetic elements such as bacteriophages. While CRISPR-Cas systems can be found throughout the prokaryotic tree of life, they are distributed unevenly across taxa and environments. Since adaptive immunity is more useful in environments where pathogens persist or reoccur, the density and/or diversity of the host/pathogen community may drive the uneven distribution of CRISPR systems. We directly tested hypotheses connecting CRISPR incidence with prokaryotic density/diversity by analyzing 16S rRNA and metagenomic data from publicly available environmental sequencing projects. In terms of density, we found that CRISPR systems are significantly favored in lower abundance (less dense) taxa and disfavored in higher abundance taxa, at least in marine environments. When we extended this work to compare taxonomic diversity between samples, we found CRISPR system incidence strongly correlated with diversity in human oral environments. Together, these observations confirm that, at least in certain types of environments, the prokaryotic ecological context indeed plays a key role in selecting for CRISPR immunity.
Importance: Microbes must constantly defend themselves against viral pathogens, and a large proportion of prokaryotes do so using the highly effective CRISPR-Cas adaptive immune system. However, many prokaryotes do not. We investigated the ecological factors behind this uneven distribution of CRISPR-Cas immune systems in natural microbial populations. We found strong patterns linking CRISPR-Cas systems to prokaryotic density within ocean environments and to prokaryotic diversity within human oral environments. Our study validates previous within-lab experimental results that suggested these factors might be important and confirms that local environment and ecological context interact to select for CRISPR immunity.
{"title":"Ecological drivers of CRISPR immune systems.","authors":"Wei Xiao, J L Weissman, Philip L F Johnson","doi":"10.1128/msystems.00568-24","DOIUrl":"10.1128/msystems.00568-24","url":null,"abstract":"<p><p>CRISPR-Cas is the only known adaptive immune system of prokaryotes. It is a powerful defense system against mobile genetic elements such as bacteriophages. While CRISPR-Cas systems can be found throughout the prokaryotic tree of life, they are distributed unevenly across taxa and environments. Since adaptive immunity is more useful in environments where pathogens persist or reoccur, the density and/or diversity of the host/pathogen community may drive the uneven distribution of CRISPR systems. We directly tested hypotheses connecting CRISPR incidence with prokaryotic density/diversity by analyzing 16S rRNA and metagenomic data from publicly available environmental sequencing projects. In terms of density, we found that CRISPR systems are significantly favored in lower abundance (less dense) taxa and disfavored in higher abundance taxa, at least in marine environments. When we extended this work to compare taxonomic diversity between samples, we found CRISPR system incidence strongly correlated with diversity in human oral environments. Together, these observations confirm that, at least in certain types of environments, the prokaryotic ecological context indeed plays a key role in selecting for CRISPR immunity.</p><p><strong>Importance: </strong>Microbes must constantly defend themselves against viral pathogens, and a large proportion of prokaryotes do so using the highly effective CRISPR-Cas adaptive immune system. However, many prokaryotes do not. We investigated the ecological factors behind this uneven distribution of CRISPR-Cas immune systems in natural microbial populations. We found strong patterns linking CRISPR-Cas systems to prokaryotic density within ocean environments and to prokaryotic diversity within human oral environments. Our study validates previous within-lab experimental results that suggested these factors might be important and confirms that local environment and ecological context interact to select for CRISPR immunity.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0056824"},"PeriodicalIF":5.0,"publicationDate":"2024-12-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11651112/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142583526","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}