Tobyn Branck, Zhiji Hu, William A Nickols, Aaron M Walsh, Amrisha Bhosle, Meghan I Short, Jacob T Nearing, Francesco Asnicar, Lauren J McIver, Sagun Maharjan, Ali Rahnavard, Artemis Louyakis, Dayakar V Badri, Christoph Brockel, Kelsey N Thompson, Curtis Huttenhower
The gut microbiome of companion animals is relatively underexplored, despite its relevance to animal health, pet owner health, and basic microbial community biology. Here, we provide the most comprehensive analysis of the canine and feline gut microbiomes to date, incorporating 2639 stool shotgun metagenomes (2272 dog and 367 cat) spanning 14 publicly available datasets (n = 730) and 8 new study populations (n = 1909). These are compared with 238 and 112 baseline human gut metagenomes from the Human Microbiome Project 1-II and a traditionally living Malagasy cohort, respectively, processed in a manner identical to the animal metagenomes. All microbiomes were characterized using reference-based taxonomic and functional profiling, as well as de novo assembly yielding metagenomic assembled genomes clustered into species-level genome bins. Companion animals shared 184 species-level genome bins not found in humans, whereas 198 were found in all three hosts. We applied novel methodology to distinguish strains of these shared organisms either transferred or unique to host species, with phylogenetic patterns suggesting host-specific adaptation of microbial lineages. This corresponded with functional divergence of these lineages by host (e.g., differences in metabolic and antibiotic resistance genes) likely important to companion animal health. This study provides the largest resource to date of companion animal gut metagenomes and greatly contributes to our understanding of the “One Health” concept of a shared microbial environment among humans and companion animals, affecting infectious diseases, immune response, and specific genetic elements.
{"title":"Comprehensive profile of the companion animal gut microbiome integrating reference-based and reference-free methods","authors":"Tobyn Branck, Zhiji Hu, William A Nickols, Aaron M Walsh, Amrisha Bhosle, Meghan I Short, Jacob T Nearing, Francesco Asnicar, Lauren J McIver, Sagun Maharjan, Ali Rahnavard, Artemis Louyakis, Dayakar V Badri, Christoph Brockel, Kelsey N Thompson, Curtis Huttenhower","doi":"10.1093/ismejo/wrae201","DOIUrl":"https://doi.org/10.1093/ismejo/wrae201","url":null,"abstract":"The gut microbiome of companion animals is relatively underexplored, despite its relevance to animal health, pet owner health, and basic microbial community biology. Here, we provide the most comprehensive analysis of the canine and feline gut microbiomes to date, incorporating 2639 stool shotgun metagenomes (2272 dog and 367 cat) spanning 14 publicly available datasets (n = 730) and 8 new study populations (n = 1909). These are compared with 238 and 112 baseline human gut metagenomes from the Human Microbiome Project 1-II and a traditionally living Malagasy cohort, respectively, processed in a manner identical to the animal metagenomes. All microbiomes were characterized using reference-based taxonomic and functional profiling, as well as de novo assembly yielding metagenomic assembled genomes clustered into species-level genome bins. Companion animals shared 184 species-level genome bins not found in humans, whereas 198 were found in all three hosts. We applied novel methodology to distinguish strains of these shared organisms either transferred or unique to host species, with phylogenetic patterns suggesting host-specific adaptation of microbial lineages. This corresponded with functional divergence of these lineages by host (e.g., differences in metabolic and antibiotic resistance genes) likely important to companion animal health. This study provides the largest resource to date of companion animal gut metagenomes and greatly contributes to our understanding of the “One Health” concept of a shared microbial environment among humans and companion animals, affecting infectious diseases, immune response, and specific genetic elements.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"229 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142430429","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cristina M Alcaraz, Joana Séneca, Martin Kunert, Christopher Pree, Marta Sudo, Jillian M Petersen
Like many marine invertebrates, marine lucinid clams have an intimate relationship with beneficial sulfur-oxidizing bacteria located within specialized gill cells known as bacteriocytes. Most previous research has focused on the symbionts in the gills of these (and other) symbiotic bivalves, often assuming that the symbionts only persistently colonize the gills, at least in the adult stage. We used 16S rRNA gene sequencing and digital polymerase chain reaction with symbiont-specific primers targeting the soxB gene on the foot, mantle, visceral mass, and gills of the lucinid clam Loripes orbiculatus. We also used fluorescence in situ hybridization with symbiont-specific probes to examine symbiont distribution at the level of the whole holobiont. Despite 40 years of research on these symbioses, we detected previously unknown populations of symbiont cells in several organs, including the digestive tract. As in the well-studied gills, symbionts in the digestive tract may be housed within host cells. A 14-month starvation experiment without hydrogen sulfide to power symbiont metabolism caused a larger reduction in symbiont numbers in the gills compared to the visceral mass, raising the possibility that symbionts in the digestive tract are persistent and may have a distinct physiology and role in the symbiosis compared with the gill symbionts. Our results highlight the unexpectedly complex relationships between marine lucinid clams and their symbionts and challenge the view that chemosynthetic symbionts are restricted to the gills of these hosts.
{"title":"Sulfur-oxidizing symbionts colonize the digestive tract of their Lucinid hosts","authors":"Cristina M Alcaraz, Joana Séneca, Martin Kunert, Christopher Pree, Marta Sudo, Jillian M Petersen","doi":"10.1093/ismejo/wrae200","DOIUrl":"https://doi.org/10.1093/ismejo/wrae200","url":null,"abstract":"Like many marine invertebrates, marine lucinid clams have an intimate relationship with beneficial sulfur-oxidizing bacteria located within specialized gill cells known as bacteriocytes. Most previous research has focused on the symbionts in the gills of these (and other) symbiotic bivalves, often assuming that the symbionts only persistently colonize the gills, at least in the adult stage. We used 16S rRNA gene sequencing and digital polymerase chain reaction with symbiont-specific primers targeting the soxB gene on the foot, mantle, visceral mass, and gills of the lucinid clam Loripes orbiculatus. We also used fluorescence in situ hybridization with symbiont-specific probes to examine symbiont distribution at the level of the whole holobiont. Despite 40 years of research on these symbioses, we detected previously unknown populations of symbiont cells in several organs, including the digestive tract. As in the well-studied gills, symbionts in the digestive tract may be housed within host cells. A 14-month starvation experiment without hydrogen sulfide to power symbiont metabolism caused a larger reduction in symbiont numbers in the gills compared to the visceral mass, raising the possibility that symbionts in the digestive tract are persistent and may have a distinct physiology and role in the symbiosis compared with the gill symbionts. Our results highlight the unexpectedly complex relationships between marine lucinid clams and their symbionts and challenge the view that chemosynthetic symbionts are restricted to the gills of these hosts.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"26 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142405075","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Katarina Belcijan Pandur, Barbara Kraigher, Ana Tomac, Polonca Stefanic, Ines Mandic Mulec
Cooperative behaviors in human, animal, and even microbial societies are vulnerable to exploitation. Kin discrimination has been hypothesized to help stabilize cooperation. However, the mechanisms that sustain cooperative behavior remain poorly understood. Here, we investigate the role of kin discrimination in limiting the spread of cheats in adjoining populations during surfactant dependent cooperative swarming over surfaces using the bacterium Bacillus subtilis as a model organism. We show that mixing surfactant secreting cooperators and cheats that do not produce surfactants at 1:1 initial ratio quickly leads to cooperation collapse. However, when such common swarms encounter non-kin B. subtilis swarms, the proportion of the surfactant non-producers decreases, suggesting that kinship dependent interactions may limit cheats’ advantage in an adjoining population. To further validate this finding, we subjected wild-type cooperators to multiple transient encounters with kin and non-kin swarms over 20 cycles of experimental evolution. The evolved populations exposed to non-kin swarms less frequently contained defective swarming phenotypes compared to those encountering kin swarms. Altogether, our results support the prediction that the spread of cheats in an adjoining bacterial population is impeded by kin discrimination interactions which might have a role in stabilizing cooperative behavior in evolving populations.
{"title":"Non-kin interactions between Bacillus subtilis soil isolates limit the spread of swarming deficient cheats","authors":"Katarina Belcijan Pandur, Barbara Kraigher, Ana Tomac, Polonca Stefanic, Ines Mandic Mulec","doi":"10.1093/ismejo/wrae199","DOIUrl":"https://doi.org/10.1093/ismejo/wrae199","url":null,"abstract":"Cooperative behaviors in human, animal, and even microbial societies are vulnerable to exploitation. Kin discrimination has been hypothesized to help stabilize cooperation. However, the mechanisms that sustain cooperative behavior remain poorly understood. Here, we investigate the role of kin discrimination in limiting the spread of cheats in adjoining populations during surfactant dependent cooperative swarming over surfaces using the bacterium Bacillus subtilis as a model organism. We show that mixing surfactant secreting cooperators and cheats that do not produce surfactants at 1:1 initial ratio quickly leads to cooperation collapse. However, when such common swarms encounter non-kin B. subtilis swarms, the proportion of the surfactant non-producers decreases, suggesting that kinship dependent interactions may limit cheats’ advantage in an adjoining population. To further validate this finding, we subjected wild-type cooperators to multiple transient encounters with kin and non-kin swarms over 20 cycles of experimental evolution. The evolved populations exposed to non-kin swarms less frequently contained defective swarming phenotypes compared to those encountering kin swarms. Altogether, our results support the prediction that the spread of cheats in an adjoining bacterial population is impeded by kin discrimination interactions which might have a role in stabilizing cooperative behavior in evolving populations.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"225 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384469","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cao Zheng, Dingqi Liu, Xinyu Lu, Huijun Wu, Jingyi Hua, Chuang Zhang, Kang Liu, Changchun Li, Jin He, Cuiying Du
The ability of bacteria to use natural carbon sources greatly affects their growth and survival in the environment. Bacteria have evolved versatile abilities to use environmental carbon sources, but their diversity and assimilation pathways remain largely unexplored. Trans-aconitic acid, a geometric isomer of cis-aconitic acid involved in the tricarboxylic acid cycle, has long been considered a natural carbon source metabolizable by bacteria. However, its catabolism and ecological role in linking bacterial interactions with the environments remain unclear. Here, we identify a regulatory system in Bacillus velezensis FZB42 that is capable of sensing and catabolizing trans-aconitic acid. The system consists of a tar operon, an adjacent positive regulatory gene tarR, and a shared promoter. After receiving the trans-aconitic acid signal, the TarR protein interacts directly with the promoter, initiating the expression of the membrane transporter TarB and aconitate isomerase TarA encoded by the operon, which function in importing the trans-aconitic acid and isomerizing it into the central intermediate cis-aconitic acid. Subsequent soil colonization experiments reveal that trans-aconitic acid assimilating ability can give its coding bacteria a growth and competitive advantage. Bioinformatics analyses coupled with bacterial isolation experiments further show that the assimilation system of trans-aconitic acid is widely distributed in the bacterial domain, and its assimilating bacteria also extensively distributed in nature, indicating an important role of trans-aconitic acid metabolism in bacterial carbon acquisition. This work emphasizes the importance of metabolic adaptation to environmental carbon sources for bacterial survival and may provide inspiration for engineering microbes with enhanced environmental competitiveness.
{"title":"Trans-aconitic acid assimilation system as a widespread bacterial mechanism for environmental adaptation","authors":"Cao Zheng, Dingqi Liu, Xinyu Lu, Huijun Wu, Jingyi Hua, Chuang Zhang, Kang Liu, Changchun Li, Jin He, Cuiying Du","doi":"10.1093/ismejo/wrae198","DOIUrl":"https://doi.org/10.1093/ismejo/wrae198","url":null,"abstract":"The ability of bacteria to use natural carbon sources greatly affects their growth and survival in the environment. Bacteria have evolved versatile abilities to use environmental carbon sources, but their diversity and assimilation pathways remain largely unexplored. Trans-aconitic acid, a geometric isomer of cis-aconitic acid involved in the tricarboxylic acid cycle, has long been considered a natural carbon source metabolizable by bacteria. However, its catabolism and ecological role in linking bacterial interactions with the environments remain unclear. Here, we identify a regulatory system in Bacillus velezensis FZB42 that is capable of sensing and catabolizing trans-aconitic acid. The system consists of a tar operon, an adjacent positive regulatory gene tarR, and a shared promoter. After receiving the trans-aconitic acid signal, the TarR protein interacts directly with the promoter, initiating the expression of the membrane transporter TarB and aconitate isomerase TarA encoded by the operon, which function in importing the trans-aconitic acid and isomerizing it into the central intermediate cis-aconitic acid. Subsequent soil colonization experiments reveal that trans-aconitic acid assimilating ability can give its coding bacteria a growth and competitive advantage. Bioinformatics analyses coupled with bacterial isolation experiments further show that the assimilation system of trans-aconitic acid is widely distributed in the bacterial domain, and its assimilating bacteria also extensively distributed in nature, indicating an important role of trans-aconitic acid metabolism in bacterial carbon acquisition. This work emphasizes the importance of metabolic adaptation to environmental carbon sources for bacterial survival and may provide inspiration for engineering microbes with enhanced environmental competitiveness.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"70 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384687","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alessandro N Garritano, Zhelun Zhang, Yunke Jia, Michelle A Allen, Lilian J Hill, Unnikrishnan Kuzhiumparambil, Cora Hinkley, Jean-Baptiste Raina, Raquel S Peixoto, Torsten Thomas
The basal metazoan phylum, Porifera (sponges), is increasingly used as a model to investigate ecological and evolutionary features of microbe-animal symbioses. However, sponges often host complex microbiomes, which has hampered our understanding of their interactions with their microbial symbionts. Here, we describe the discovery and characterisation of the simplest sponge holobiont reported to date, consisting of the deep-sea glass sponge Aphrocalistes beatrix and two newly described microbial symbionts: an autotrophic ammonia-oxidising archaeon and a bacterial heterotroph. Omics analyses and metabolic modelling revealed the dependency of the ammonia-oxidising archaea on sponge-derived ammonia to drive primary production, which in turn supports the bacterium’s growth by providing the dicarboxylate fumarate. Furthermore, virus-mediated archaeal lysis appears crucial to overcome the bacterium’s vitamin B12 auxotrophy. These findings reveal that the exchange of vitamin B12 and dicarboxylate may be evolutionarily conserved features of symbiosis as they can also be found in interactions between free-living marine bacteria, and between microbes and plants or diatoms.
{"title":"Simple Porifera holobiont reveals complex interactions between the host, an archaeon, a bacterium, and a phage","authors":"Alessandro N Garritano, Zhelun Zhang, Yunke Jia, Michelle A Allen, Lilian J Hill, Unnikrishnan Kuzhiumparambil, Cora Hinkley, Jean-Baptiste Raina, Raquel S Peixoto, Torsten Thomas","doi":"10.1093/ismejo/wrae197","DOIUrl":"https://doi.org/10.1093/ismejo/wrae197","url":null,"abstract":"The basal metazoan phylum, Porifera (sponges), is increasingly used as a model to investigate ecological and evolutionary features of microbe-animal symbioses. However, sponges often host complex microbiomes, which has hampered our understanding of their interactions with their microbial symbionts. Here, we describe the discovery and characterisation of the simplest sponge holobiont reported to date, consisting of the deep-sea glass sponge Aphrocalistes beatrix and two newly described microbial symbionts: an autotrophic ammonia-oxidising archaeon and a bacterial heterotroph. Omics analyses and metabolic modelling revealed the dependency of the ammonia-oxidising archaea on sponge-derived ammonia to drive primary production, which in turn supports the bacterium’s growth by providing the dicarboxylate fumarate. Furthermore, virus-mediated archaeal lysis appears crucial to overcome the bacterium’s vitamin B12 auxotrophy. These findings reveal that the exchange of vitamin B12 and dicarboxylate may be evolutionarily conserved features of symbiosis as they can also be found in interactions between free-living marine bacteria, and between microbes and plants or diatoms.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"64 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384703","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Qian Yang, Yin Zhong, Shi-wei Feng, Ping Wen, Heli Wang, Junhong Wu, Sen Yang, Jie-Liang Liang, Dan Li, Qiong Yang, Nora F Y Tam, Ping’an Peng
Plastic marine debris is known to harbor a unique microbiome (termed the “plastisphere”) that can be important in marine biogeochemical cycles. However, the temporal dynamics in the plastisphere and their implications for marine biogeochemistry remain poorly understood. Here, we characterized the temporal dynamics of nitrifying communities in the plastisphere of plastic ropes exposed to a mangrove intertidal zone. The 39-month colonization experiment revealed that the relative abundances of Nitrospira and Candidatus Nitrosocosmicus representatives increased over time according to 16S rRNA gene amplicon sequencing analysis. The relative abundances of amoA genes in metagenomes implied that comammox Nitrospira were the dominant ammonia oxidizers in the plastisphere, and their dominance increased over time. The relative abundances of two metagenome-assembled genomes of comammox Nitrospira also increased with time and positively correlated with extracellular polymeric substances content of the plastisphere but negatively correlated with NH4+ concentration in seawater, indicating the long-term succession of these two parameters significantly influenced the ammonia-oxidizing community in the coastal plastisphere. At the end of the colonization experiment, the plastisphere exhibited high nitrification activity, leading to the release of N2O (2.52 ng N2O N g−1) in a 3-day nitrification experiment. The predicted relative contribution of comammox Nitrospira to N2O production (17.9%) was higher than that of ammonia-oxidizing bacteria (4.8%) but lower than that of ammonia-oxidizing archaea (21.4%). These results provide evidence that from a long-term perspective, some coastal plastispheres will become dominated by comammox Nitrospira and thereby act as hotspots of ammonia oxidation and N2O production.
众所周知，海洋塑料废弃物蕴藏着一个独特的微生物群落（称为 "质圈"），在海洋生物地球化学循环中可能非常重要。然而，人们对塑料海洋废弃物的时间动态及其对海洋生物地球化学的影响仍然知之甚少。在这里，我们描述了暴露在红树林潮间带的塑料绳塑性层中硝化群落的时间动态。为期 39 个月的定殖实验表明，根据 16S rRNA 基因扩增片段测序分析，硝化细菌（Nitrospira）和硝化球菌（Candidatus Nitrosocosmicus）代表的相对丰度随着时间的推移而增加。元基因组中amoA基因的相对丰度表明，复合氧化硝化梭菌是质球中最主要的氨氧化剂，而且其优势地位随着时间的推移而增加。comammox硝基螺杆菌的两个元基因组组装基因的相对丰度也随着时间的推移而增加，并与质球的胞外聚合物质含量呈正相关，但与海水中的NH4+浓度呈负相关，表明这两个参数的长期演替对沿岸质球的氨氧化群落有显著影响。在定殖实验结束时，质球表现出很高的硝化活性，在为期 3 天的硝化实验中释放出 N2O（2.52 ng N2O N g-1）。预计复合氧化硝化弧菌对 N2O 产量的相对贡献率（17.9%）高于氨氧化细菌（4.8%），但低于氨氧化古细菌（21.4%）。这些结果证明，从长远角度看，一些沿岸块根动物将以兼氧硝化纤维为主，从而成为氨氧化和产生 N2O 的热点。
{"title":"Temporal enrichment of comammox Nitrospira and Ca. Nitrosocosmicus in a coastal plastisphere","authors":"Qian Yang, Yin Zhong, Shi-wei Feng, Ping Wen, Heli Wang, Junhong Wu, Sen Yang, Jie-Liang Liang, Dan Li, Qiong Yang, Nora F Y Tam, Ping’an Peng","doi":"10.1093/ismejo/wrae186","DOIUrl":"https://doi.org/10.1093/ismejo/wrae186","url":null,"abstract":"Plastic marine debris is known to harbor a unique microbiome (termed the “plastisphere”) that can be important in marine biogeochemical cycles. However, the temporal dynamics in the plastisphere and their implications for marine biogeochemistry remain poorly understood. Here, we characterized the temporal dynamics of nitrifying communities in the plastisphere of plastic ropes exposed to a mangrove intertidal zone. The 39-month colonization experiment revealed that the relative abundances of Nitrospira and Candidatus Nitrosocosmicus representatives increased over time according to 16S rRNA gene amplicon sequencing analysis. The relative abundances of amoA genes in metagenomes implied that comammox Nitrospira were the dominant ammonia oxidizers in the plastisphere, and their dominance increased over time. The relative abundances of two metagenome-assembled genomes of comammox Nitrospira also increased with time and positively correlated with extracellular polymeric substances content of the plastisphere but negatively correlated with NH4+ concentration in seawater, indicating the long-term succession of these two parameters significantly influenced the ammonia-oxidizing community in the coastal plastisphere. At the end of the colonization experiment, the plastisphere exhibited high nitrification activity, leading to the release of N2O (2.52 ng N2O N g−1) in a 3-day nitrification experiment. The predicted relative contribution of comammox Nitrospira to N2O production (17.9%) was higher than that of ammonia-oxidizing bacteria (4.8%) but lower than that of ammonia-oxidizing archaea (21.4%). These results provide evidence that from a long-term perspective, some coastal plastispheres will become dominated by comammox Nitrospira and thereby act as hotspots of ammonia oxidation and N2O production.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"12 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384694","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Tingwei Cai, Pol Nadal-Jimenez, Yuanyuan Gao, Hiroshi Arai, Chengyue Li, Chunyan Su, Kayla C King, Shun He, Jianhong Li, Gregory D D Hurst, Hu Wan
Facultative vertically transmitted symbionts are a common feature of insects that determine many aspects of their hosts’ phenotype. Our capacity to understand and exploit these symbioses is commonly compromised by the microbes unculturability and consequent lack of genetic tools, an impediment of particular significance for symbioses of pest and vector species. Previous work had established that insecticide susceptibility of the economically important pest of rice, the brown planthopper Nilaparvata lugens, was higher in field-collected lineages that carry Ca. Arsenophonus nilaparvatae. We established Ca. A. nilaparvatae into cell-free culture and used this to establish the complete closed genome of the symbiont. We transformed the strain to express GFP and reintroduced it to N. lugens to track infection in vivo. The symbiont established vertical transmission, generating a discrete infection focus towards the posterior pole of each N. lugens oocyte. This infection focus was retained in early embryogenesis before transition to a diffuse somatic infection in late N. lugens embryos and nymphs. We additionally generated somatic infection in novel host species, but these did not establish vertical transmission. Transinfected planthopper lines acquired the insecticide sensitivity trait, with associated downregulation of the P450 xenobiotic detoxification system of the host. Our results causally establish the role of the symbiont in increasing host insecticide sensitivity with implications for insecticide use and stewardship. Further, the culturability and transformation of this intracellular symbiont, combined with its ease of reintroduction to planthopper hosts, enables novel approaches both for research into symbiosis and into control of insect pest species.
兼性垂直传播共生体是昆虫的一个共同特征，它决定了宿主表型的许多方面。我们了解和利用这些共生体的能力通常受到微生物不可培养性和随之而来的遗传工具缺乏的影响，这一障碍对于害虫和病媒物种的共生体尤为重要。以前的工作已经证实，对水稻具有重要经济价值的害虫--褐飞虱 Nilaparvata lugens--的杀虫剂敏感性在携带 Ca.Arsenophonus nilaparvatae。我们确定了 Ca.nilaparvatae 的无细胞培养，并以此建立了共生体的完整封闭基因组。我们将该菌株转化为表达 GFP 的菌株，并将其重新引入 N. lugens，以追踪体内感染情况。该共生体建立了垂直传播，在每个 N. lugens 卵母细胞的后极产生了一个离散的感染灶。在 N. lugens 胚胎和若虫后期过渡到弥漫性体细胞感染之前，这一感染病灶在早期胚胎发育过程中一直存在。我们还在新的宿主物种中产生了体细胞感染，但这些感染并未建立垂直传播。经转染的花斑叶蝉品系获得了对杀虫剂敏感的性状，宿主的 P450 异生物解毒系统也随之下调。我们的研究结果从因果关系上确定了共生体在提高宿主杀虫剂敏感性方面的作用，对杀虫剂的使用和管理具有重要意义。此外，这种细胞内共生体的可培养性和可转化性，再加上它易于被重新引入到栉水母宿主体内，使得共生研究和昆虫害虫控制都有了新的方法。
{"title":"Insecticide susceptibility in a planthopper pest increases following inoculation with cultured Arsenophonus","authors":"Tingwei Cai, Pol Nadal-Jimenez, Yuanyuan Gao, Hiroshi Arai, Chengyue Li, Chunyan Su, Kayla C King, Shun He, Jianhong Li, Gregory D D Hurst, Hu Wan","doi":"10.1093/ismejo/wrae194","DOIUrl":"https://doi.org/10.1093/ismejo/wrae194","url":null,"abstract":"Facultative vertically transmitted symbionts are a common feature of insects that determine many aspects of their hosts’ phenotype. Our capacity to understand and exploit these symbioses is commonly compromised by the microbes unculturability and consequent lack of genetic tools, an impediment of particular significance for symbioses of pest and vector species. Previous work had established that insecticide susceptibility of the economically important pest of rice, the brown planthopper Nilaparvata lugens, was higher in field-collected lineages that carry Ca. Arsenophonus nilaparvatae. We established Ca. A. nilaparvatae into cell-free culture and used this to establish the complete closed genome of the symbiont. We transformed the strain to express GFP and reintroduced it to N. lugens to track infection in vivo. The symbiont established vertical transmission, generating a discrete infection focus towards the posterior pole of each N. lugens oocyte. This infection focus was retained in early embryogenesis before transition to a diffuse somatic infection in late N. lugens embryos and nymphs. We additionally generated somatic infection in novel host species, but these did not establish vertical transmission. Transinfected planthopper lines acquired the insecticide sensitivity trait, with associated downregulation of the P450 xenobiotic detoxification system of the host. Our results causally establish the role of the symbiont in increasing host insecticide sensitivity with implications for insecticide use and stewardship. Further, the culturability and transformation of this intracellular symbiont, combined with its ease of reintroduction to planthopper hosts, enables novel approaches both for research into symbiosis and into control of insect pest species.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"12 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142384701","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jiadong He, Lin Zhang, Judith Van Dingenen, Sandrien Desmet, Sofie Goormachtig, Maryline Calonne-Salmon, Stéphane Declerck
In soil ecosystems, rhizobia occupy the rhizosphere of legume roots to form nodules, a process triggered by microbial recognition of specific root-derived signals (i.e., flavonoids). However, soil conditions can limit bacterial motility, restricting signal perception to the area directly influenced by roots. Legumes, like most plants of agricultural interest, associate with arbuscular mycorrhizal fungi, whose hyphae develop extensively in the soil, potentially providing an effective dispersal network for rhizobia. We hypothesized that mycelial networks of arbuscular mycorrhizal fungi play a role in signal transmission and act as a highway, enabling rhizobia to migrate from distant soil to the roots of leguminous plants. Using in vitro and greenhouse microcosm systems, we demonstrated that Rhizophagus irregularis helps Shinorhizobium meliloti to migrate towards the legume Medicago truncatula, triggering nodulation, a mechanism absent without the arbuscular mycorrhizal fungus. Metabolomics analysis revealed eight flavonoids unique to the compartment containing extraradical hyphae of the arbuscular mycorrhizal fungus linked to M. truncatula roots, associated with S. meliloti growth and nod gene expression. Rhizobia plated on the extraradical hyphae connecting two plants (the legume M. truncatula and non-legume Solanum tuberosum) by a common mycelium network, showed preference for the legume, suggesting the chemoattraction by specific signals transported by the fungus connected to the legume. Simultaneously, S. meliloti stimulated the cytoplasmic/protoplasmic flow in the hyphae, likely increasing the release of nutrients and signals. Our results highlight the importance of extraradical hyphae (i.e. the mycorrhizal pathway) of arbuscular mycorrhizal fungi for the migration of rhizobia over long distances to the roots, leading to nodulation.
{"title":"Arbuscular mycorrhizal hyphae facilitate rhizobia dispersal and nodulation in legumes","authors":"Jiadong He, Lin Zhang, Judith Van Dingenen, Sandrien Desmet, Sofie Goormachtig, Maryline Calonne-Salmon, Stéphane Declerck","doi":"10.1093/ismejo/wrae185","DOIUrl":"https://doi.org/10.1093/ismejo/wrae185","url":null,"abstract":"In soil ecosystems, rhizobia occupy the rhizosphere of legume roots to form nodules, a process triggered by microbial recognition of specific root-derived signals (i.e., flavonoids). However, soil conditions can limit bacterial motility, restricting signal perception to the area directly influenced by roots. Legumes, like most plants of agricultural interest, associate with arbuscular mycorrhizal fungi, whose hyphae develop extensively in the soil, potentially providing an effective dispersal network for rhizobia. We hypothesized that mycelial networks of arbuscular mycorrhizal fungi play a role in signal transmission and act as a highway, enabling rhizobia to migrate from distant soil to the roots of leguminous plants. Using in vitro and greenhouse microcosm systems, we demonstrated that Rhizophagus irregularis helps Shinorhizobium meliloti to migrate towards the legume Medicago truncatula, triggering nodulation, a mechanism absent without the arbuscular mycorrhizal fungus. Metabolomics analysis revealed eight flavonoids unique to the compartment containing extraradical hyphae of the arbuscular mycorrhizal fungus linked to M. truncatula roots, associated with S. meliloti growth and nod gene expression. Rhizobia plated on the extraradical hyphae connecting two plants (the legume M. truncatula and non-legume Solanum tuberosum) by a common mycelium network, showed preference for the legume, suggesting the chemoattraction by specific signals transported by the fungus connected to the legume. Simultaneously, S. meliloti stimulated the cytoplasmic/protoplasmic flow in the hyphae, likely increasing the release of nutrients and signals. Our results highlight the importance of extraradical hyphae (i.e. the mycorrhizal pathway) of arbuscular mycorrhizal fungi for the migration of rhizobia over long distances to the roots, leading to nodulation.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"217 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325510","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Cécile Gubry-Rangin, Axel Aigle, Leonel Herrera-Alsina, Lesley T Lancaster, James I Prosser
None declared.Conflicts of interestEcological theory predicts that organismal distribution and abundance depend on the ability to adapt to environmental change. It also predicts that eukaryotic specialists and generalists will dominate in extreme environments or following environmental change, respectively. This theory has attracted little attention in prokaryotes, especially in archaea, which drive major global biogeochemical cycles. We tested this concept in Thaumarchaeota using pH niche breadth as a specialisation factor. Responses of archaeal growth and activity to pH disturbance were determined empirically in manipulated, long-term, pH-maintained soil plots. The distribution of specialists and generalists was uneven over the pH range, with specialists being more limited to the extreme range. Nonetheless, adaptation of generalists to environmental change was greater than that of specialists, except for environmental changes leading to more extreme conditions. The balance of generalism and specialism over longer timescales was further investigated across evolutionary history. Specialists and generalists diversified at similar rates, reflecting balanced benefits of each strategy, but a higher transition rate from generalists to specialists than the reverse was demonstrated, suggesting that metabolic specialism is more easily gained than metabolic versatility. This study provides evidence for a crucial ecological concept in prokaryotes, significantly extending our understanding of archaeal adaptation to environmental change.
{"title":"Niche breadth specialisation impacts ecological and evolutionary adaptation following environmental change","authors":"Cécile Gubry-Rangin, Axel Aigle, Leonel Herrera-Alsina, Lesley T Lancaster, James I Prosser","doi":"10.1093/ismejo/wrae183","DOIUrl":"https://doi.org/10.1093/ismejo/wrae183","url":null,"abstract":"None declared.Conflicts of interestEcological theory predicts that organismal distribution and abundance depend on the ability to adapt to environmental change. It also predicts that eukaryotic specialists and generalists will dominate in extreme environments or following environmental change, respectively. This theory has attracted little attention in prokaryotes, especially in archaea, which drive major global biogeochemical cycles. We tested this concept in Thaumarchaeota using pH niche breadth as a specialisation factor. Responses of archaeal growth and activity to pH disturbance were determined empirically in manipulated, long-term, pH-maintained soil plots. The distribution of specialists and generalists was uneven over the pH range, with specialists being more limited to the extreme range. Nonetheless, adaptation of generalists to environmental change was greater than that of specialists, except for environmental changes leading to more extreme conditions. The balance of generalism and specialism over longer timescales was further investigated across evolutionary history. Specialists and generalists diversified at similar rates, reflecting balanced benefits of each strategy, but a higher transition rate from generalists to specialists than the reverse was demonstrated, suggesting that metabolic specialism is more easily gained than metabolic versatility. This study provides evidence for a crucial ecological concept in prokaryotes, significantly extending our understanding of archaeal adaptation to environmental change.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"55 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325511","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Elizabeth C Cooney, Brian S Leander, Patrick J Keeling
Free-living core dinoflagellates are commonly infected by members of two parasitic clades that are themselves closely related to dinoflagellates, the marine alveolates and perkinsids. These parasites are abundant and ecologically important, but most species have been difficult to observe directly or cultivate, so our knowledge of them is usually restricted to environmental 18S rRNA gene sequences, and genome-scale molecular data are not available for most species. Here, we report numerous syndinian parasites and one parasite that is sister to all known perkinsids from isolated single cells of diverse, free-living dinoflagellates. Of the 14 infected host cells collected, only five were noticeably infected via light microscopy at the time of collection. Single-cell transcriptome sequencing yielded relatively high transcriptomic coverage for parasites as well as their hosts. Host and parasite homologs were distinguished phylogenetically allowing us to infer a robust phylogenomic tree based on 198 genes. The tree showed one parasite belongs to an undescribed lineage that is sister to perkinsids, whereas the remainder are members of the syndinian clade. Close relatives of all these parasites have been observed in 18S rRNA gene surveys, but until now none had been linked to a specific host. These findings illustrate the efficacy of single-cell isolation and transcriptome sequencing as a strategy for gaining deeper insights into the evolutionary history and host relationships of hidden single-celled parasites.
{"title":"Hidden syndinian and perkinsid infections in dinoflagellate hosts revealed by single-cell transcriptomics","authors":"Elizabeth C Cooney, Brian S Leander, Patrick J Keeling","doi":"10.1093/ismejo/wrae188","DOIUrl":"https://doi.org/10.1093/ismejo/wrae188","url":null,"abstract":"Free-living core dinoflagellates are commonly infected by members of two parasitic clades that are themselves closely related to dinoflagellates, the marine alveolates and perkinsids. These parasites are abundant and ecologically important, but most species have been difficult to observe directly or cultivate, so our knowledge of them is usually restricted to environmental 18S rRNA gene sequences, and genome-scale molecular data are not available for most species. Here, we report numerous syndinian parasites and one parasite that is sister to all known perkinsids from isolated single cells of diverse, free-living dinoflagellates. Of the 14 infected host cells collected, only five were noticeably infected via light microscopy at the time of collection. Single-cell transcriptome sequencing yielded relatively high transcriptomic coverage for parasites as well as their hosts. Host and parasite homologs were distinguished phylogenetically allowing us to infer a robust phylogenomic tree based on 198 genes. The tree showed one parasite belongs to an undescribed lineage that is sister to perkinsids, whereas the remainder are members of the syndinian clade. Close relatives of all these parasites have been observed in 18S rRNA gene surveys, but until now none had been linked to a specific host. These findings illustrate the efficacy of single-cell isolation and transcriptome sequencing as a strategy for gaining deeper insights into the evolutionary history and host relationships of hidden single-celled parasites.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"3 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142325509","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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