Lin Chen, Xue Zhao, Shelyn Wongso, Zhuohui Lin, Siyun Wang
Parasite–host co-evolution results in population extinction or co-existence, yet the factors driving these distinct outcomes remain elusive. In this study, Salmonella strains were individually co-evolved with the lytic phage SF1 for 30 days, resulting in phage extinction or co-existence. We conducted a systematic investigation into the phenotypic and genetic dynamics of evolved host cells and phages to elucidate the evolutionary mechanisms. Throughout co-evolution, host cells displayed diverse phage resistance patterns: sensitivity, partial resistance, and complete resistance, to wild-type phage. Moreover, phage resistance strength showed a robust linear correlation with phage adsorption, suggesting that surface modification-mediated phage attachment predominates as the resistance mechanism in evolved bacterial populations. Additionally, bacterial isolates eliminating phages exhibited higher mutation rates and lower fitness costs in developing resistance compared to those leading to co-existence. Phage resistance genes were classified into two categories: key mutations, characterized by nonsense/frameshift mutations in rfaH-regulated rfb genes, leading to the removal of the receptor O-antigen; and secondary mutations, which involve less critical modifications, such as fimbrial synthesis and tRNA modification. The accumulation of secondary mutations resulted in partial and complete resistance, which could be overcome by evolved phages, whereas key mutations conferred undefeatable complete resistance by deleting receptors. In conclusion, higher key mutation frequencies with lower fitness costs promised strong resistance and eventual phage extinction, whereas deficiencies in fitness cost, mutation rate, and key mutation led to co-existence. Our findings reveal the distinct population dynamics and evolutionary trade-offs of phage resistance during co-evolution, thereby deepening our understanding of microbial interactions.
{"title":"Trade-offs between receptor modification and fitness drive host-bacteriophage co-evolution leading to phage extinction or co-existence","authors":"Lin Chen, Xue Zhao, Shelyn Wongso, Zhuohui Lin, Siyun Wang","doi":"10.1093/ismejo/wrae214","DOIUrl":"https://doi.org/10.1093/ismejo/wrae214","url":null,"abstract":"Parasite–host co-evolution results in population extinction or co-existence, yet the factors driving these distinct outcomes remain elusive. In this study, Salmonella strains were individually co-evolved with the lytic phage SF1 for 30 days, resulting in phage extinction or co-existence. We conducted a systematic investigation into the phenotypic and genetic dynamics of evolved host cells and phages to elucidate the evolutionary mechanisms. Throughout co-evolution, host cells displayed diverse phage resistance patterns: sensitivity, partial resistance, and complete resistance, to wild-type phage. Moreover, phage resistance strength showed a robust linear correlation with phage adsorption, suggesting that surface modification-mediated phage attachment predominates as the resistance mechanism in evolved bacterial populations. Additionally, bacterial isolates eliminating phages exhibited higher mutation rates and lower fitness costs in developing resistance compared to those leading to co-existence. Phage resistance genes were classified into two categories: key mutations, characterized by nonsense/frameshift mutations in rfaH-regulated rfb genes, leading to the removal of the receptor O-antigen; and secondary mutations, which involve less critical modifications, such as fimbrial synthesis and tRNA modification. The accumulation of secondary mutations resulted in partial and complete resistance, which could be overcome by evolved phages, whereas key mutations conferred undefeatable complete resistance by deleting receptors. In conclusion, higher key mutation frequencies with lower fitness costs promised strong resistance and eventual phage extinction, whereas deficiencies in fitness cost, mutation rate, and key mutation led to co-existence. Our findings reveal the distinct population dynamics and evolutionary trade-offs of phage resistance during co-evolution, thereby deepening our understanding of microbial interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"211 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488818","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}
Catie S Cleveland, Kendra A Turk-Kubo, Yiming Zhao, Jonathan P Zehr, Eric A Webb
Marine N2-fixing cyanobacteria, including the unicellular genus Crocosphaera, are considered keystone species in marine food webs. Crocosphaera are globally distributed and provide new sources of nitrogen and carbon, which fuel oligotrophic microbial communities and upper trophic levels. Despite their ecosystem importance, only one pelagic, oligotrophic, phycoerythrin-rich species, Crocosphaera watsonii, has ever been identified and characterized as widespread. Herein, we present a new species, named Crocosphaera waterburyi, enriched from the North Pacific Ocean. C. waterburyi was found to be phenotypically and genotypically distinct from C. watsonii, active in situ, distributed globally, and preferred warmer temperatures in culture and the ocean. Additionally, C. waterburyi was detectable in 150- and 4000-meter sediment export traps, had a relatively larger biovolume than C. watsonii, and appeared to aggregate in the environment and laboratory culture. Therefore, it represents an additional, previously unknown link between atmospheric CO2 and N2 gas and deep ocean carbon and nitrogen export and sequestration.
海洋固氮蓝藻（包括单细胞蓝藻属）被认为是海洋食物网中的关键物种。Crocosphaera分布于全球，提供新的氮和碳源，为低营养微生物群落和上层营养级提供动力。尽管它们在生态系统中非常重要，但目前仅发现了一种富含藻红素的中上层低营养物种--Crocosphaera watsonii，并将其描述为广泛分布的物种。在此，我们介绍了一个来自北太平洋的新物种，名为 Crocosphaera waterburyi。研究发现，C. waterburyi 在表型和基因型上都与 C. watsonii 不同，它在原地活动，分布于全球各地，在养殖和海洋中喜欢较高的温度。此外，在 150 米和 4000 米的沉积物出口捕集器中可以检测到 C. waterburyi，它的生物体积比 C. watsonii 大，而且似乎在环境和实验室培养中聚集在一起。因此，它代表了大气中的二氧化碳和二氧化氮气体与深海碳和氮的输出和螯合之间的另一种以前未知的联系。
{"title":"Marine N2-fixer Crocosphaera waterburyi","authors":"Catie S Cleveland, Kendra A Turk-Kubo, Yiming Zhao, Jonathan P Zehr, Eric A Webb","doi":"10.1093/ismejo/wrae217","DOIUrl":"https://doi.org/10.1093/ismejo/wrae217","url":null,"abstract":"Marine N2-fixing cyanobacteria, including the unicellular genus Crocosphaera, are considered keystone species in marine food webs. Crocosphaera are globally distributed and provide new sources of nitrogen and carbon, which fuel oligotrophic microbial communities and upper trophic levels. Despite their ecosystem importance, only one pelagic, oligotrophic, phycoerythrin-rich species, Crocosphaera watsonii, has ever been identified and characterized as widespread. Herein, we present a new species, named Crocosphaera waterburyi, enriched from the North Pacific Ocean. C. waterburyi was found to be phenotypically and genotypically distinct from C. watsonii, active in situ, distributed globally, and preferred warmer temperatures in culture and the ocean. Additionally, C. waterburyi was detectable in 150- and 4000-meter sediment export traps, had a relatively larger biovolume than C. watsonii, and appeared to aggregate in the environment and laboratory culture. Therefore, it represents an additional, previously unknown link between atmospheric CO2 and N2 gas and deep ocean carbon and nitrogen export and sequestration.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"35 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488816","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}
Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven’t been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.
{"title":"Taeniasis impacts human gut microbiome composition and function","authors":"Wenjie Mu, Pingping Ma, Yugui Wang, Yaqi Li, Yingying Ding, Yang Zou, Lixia Pu, Qi Yan, Haoyue Kong, Xiaola Guo, Aijiang Guo, Hailong Li, Shuai Wang","doi":"10.1093/ismejo/wrae213","DOIUrl":"https://doi.org/10.1093/ismejo/wrae213","url":null,"abstract":"Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven’t been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"235 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488823","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}
Sang-Moo Lee, Roniya Thapa Magar, Min Kyeong Jung, Hyun Gi Kong, Ju Yeon Song, Joo Hwan Kwon, Minseo Choi, Hyoung Ju Lee, Seung Yeup Lee, Raees Khan, Jihyun F Kim, Seon-Woo Lee
None declared.Conflicts of interestMicrobial interactions impact the functioning of microbial communities. However, microbial interactions within host-associated communities remains poorly understood. Here, we report that the beneficiary rhizobacterium Niallia sp. RD1 requires the helper Pseudomonas putida H3 for bacterial growth and beneficial interactions with the plant host. In the absence of the helper H3 strain, the Niallia sp. RD1 strain exhibited weak respiration and elongated cell morphology without forming bacterial colonies. A transposon mutant of H3 in a gene encoding succinate-semialdehyde dehydrogenase displayed much attenuated support of RD1 colony formation. Through subsequent addition of succinate to the media, we found that succinate serves as a public good that supports RD1 growth. Comparative genome analysis highlighted that RD1 lacked the gene for sufficient succinate, suggesting its evolution as a beneficiary of succinate biosynthesis. The syntrophic interaction between RD1 and H3 efficiently protected tomato plants from bacterial wilt and promoted the tomato growth. The addition of succinate to the medium restored complex II-dependent respiration in RD1 and facilitated the cultivation of various bacterial isolates from the rhizosphere. Taken together, we delineate energy auxotrophic beneficiaries ubiquitous in the microbial community, and these beneficiaries could benefit host plants with the aid of helpers in the rhizosphere.
{"title":"Rhizobacterial syntrophy between a helper and a beneficiary promotes tomato plant health","authors":"Sang-Moo Lee, Roniya Thapa Magar, Min Kyeong Jung, Hyun Gi Kong, Ju Yeon Song, Joo Hwan Kwon, Minseo Choi, Hyoung Ju Lee, Seung Yeup Lee, Raees Khan, Jihyun F Kim, Seon-Woo Lee","doi":"10.1093/ismejo/wrae210","DOIUrl":"https://doi.org/10.1093/ismejo/wrae210","url":null,"abstract":"None declared.Conflicts of interestMicrobial interactions impact the functioning of microbial communities. However, microbial interactions within host-associated communities remains poorly understood. Here, we report that the beneficiary rhizobacterium Niallia sp. RD1 requires the helper Pseudomonas putida H3 for bacterial growth and beneficial interactions with the plant host. In the absence of the helper H3 strain, the Niallia sp. RD1 strain exhibited weak respiration and elongated cell morphology without forming bacterial colonies. A transposon mutant of H3 in a gene encoding succinate-semialdehyde dehydrogenase displayed much attenuated support of RD1 colony formation. Through subsequent addition of succinate to the media, we found that succinate serves as a public good that supports RD1 growth. Comparative genome analysis highlighted that RD1 lacked the gene for sufficient succinate, suggesting its evolution as a beneficiary of succinate biosynthesis. The syntrophic interaction between RD1 and H3 efficiently protected tomato plants from bacterial wilt and promoted the tomato growth. The addition of succinate to the medium restored complex II-dependent respiration in RD1 and facilitated the cultivation of various bacterial isolates from the rhizosphere. Taken together, we delineate energy auxotrophic beneficiaries ubiquitous in the microbial community, and these beneficiaries could benefit host plants with the aid of helpers in the rhizosphere.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"13 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142487603","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}
Kerrin Steensen, Joana Séneca, Nina Bartlau, Xiaoqian A Yu, Fatima A Hussain, Martin F Polz
Although tailed bacteriophages (phages) of the class Caudoviricetes are thought to constitute the most abundant and ecologically relevant group of phages that can integrate their genome into the host chromosome, it is becoming increasingly clear that other prophages are widespread. Here, we show that prophages derived from filamentous and tailless phages with genome sizes below 16 kb make up the majority of prophages in marine bacteria of the genus Vibrio. To estimate prophage prevalence unaffected by database biases, we combined comparative genomics and chemical induction of 58 diverse Vibrio cyclitrophicus isolates, resulting in 107 well-curated prophages. Complemented with computationally predicted prophages, we obtained 1,158 prophages from 931 naturally co-existing strains of the family Vibrionaceae. Prophages resembling tailless and filamentous phages predominated, accounting for 80% of all prophages in V. cyclitrophicus and 60% across the Vibrionaceae. In our experimental model, prophages of all three viral realms actively replicated upon induction indicating their ability to transfer to new hosts. Indeed, prophages were rapidly gained and lost, as suggested by variable prophage content between closely related V. cyclitrophicus. Prophages related to filamentous and tailless phages were integrated into only three genomic locations and restored the function of their integration site. Despite their small size, they contained highly diverse accessory genes that may contribute to host fitness, such as phage defense systems. We propose that, like their well-studied tailed equivalent, tailless and filamentous temperate phages are active and highly abundant drivers of host ecology and evolution in marine Vibrio, which have been largely overlooked.
{"title":"Prophages in Vibrio","authors":"Kerrin Steensen, Joana Séneca, Nina Bartlau, Xiaoqian A Yu, Fatima A Hussain, Martin F Polz","doi":"10.1093/ismejo/wrae202","DOIUrl":"https://doi.org/10.1093/ismejo/wrae202","url":null,"abstract":"Although tailed bacteriophages (phages) of the class Caudoviricetes are thought to constitute the most abundant and ecologically relevant group of phages that can integrate their genome into the host chromosome, it is becoming increasingly clear that other prophages are widespread. Here, we show that prophages derived from filamentous and tailless phages with genome sizes below 16 kb make up the majority of prophages in marine bacteria of the genus Vibrio. To estimate prophage prevalence unaffected by database biases, we combined comparative genomics and chemical induction of 58 diverse Vibrio cyclitrophicus isolates, resulting in 107 well-curated prophages. Complemented with computationally predicted prophages, we obtained 1,158 prophages from 931 naturally co-existing strains of the family Vibrionaceae. Prophages resembling tailless and filamentous phages predominated, accounting for 80% of all prophages in V. cyclitrophicus and 60% across the Vibrionaceae. In our experimental model, prophages of all three viral realms actively replicated upon induction indicating their ability to transfer to new hosts. Indeed, prophages were rapidly gained and lost, as suggested by variable prophage content between closely related V. cyclitrophicus. Prophages related to filamentous and tailless phages were integrated into only three genomic locations and restored the function of their integration site. Despite their small size, they contained highly diverse accessory genes that may contribute to host fitness, such as phage defense systems. We propose that, like their well-studied tailed equivalent, tailless and filamentous temperate phages are active and highly abundant drivers of host ecology and evolution in marine Vibrio, which have been largely overlooked.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"4 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142449618","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}
Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer
Quickly after birth, the gut microbiota is shaped via species acquisition and resource pressure. Breastmilk, and more specifically, human milk oligosaccharides are a determining factor in the formation of microbial communities and the interactions between bacteria. Prominent human milk oligosaccharide degraders have been rigorously characterized, but it is not known how the gut microbiota is shaped as a complex community. Here, we designed BIG-Syc, a synthetic community of 13 strains from the gut of vaginally born, breastfed infants. BIG-Syc replicated key compositional, metabolic, and proteomic characteristics of the gut microbiota of infants. Upon fermentation of a 4 and 5 human milk oligosaccharide mix, BIG-Syc demonstrated different compositional and proteomic profiles, with Bifidobacterium infantis and Bifidobacterium bifidum suppressing one another. The mix of 5 human milk oligosaccharides resulted in a more diverse composition with dominance of B. bifidum, whereas that with 4 human milk oligosaccharides supported the dominance of B. infantis, in 4 of 6 replicates. Reintroduction of bifidobacteria to BIG-Syc led to their engraftment and establishment of their niche. Based on proteomics and genome-scale metabolic models, we reconstructed the carbon source utilization and metabolite and gas production per strain. BIG-Syc demonstrated teamwork as cross-feeders utilized simpler carbohydrates, organic acids, and gases released from human milk oligosaccharide degraders. Collectively, our results showed that human milk oligosaccharides prompt resource-sharing for their complete degradation while leading to a different compositional and functional profile in the community. At the same time, BIG-Syc proved to be an accurate model for the representation of intra-microbe interactions.
{"title":"Resource sharing of an infant gut microbiota synthetic community in combinations of human milk oligosaccharides","authors":"Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer","doi":"10.1093/ismejo/wrae209","DOIUrl":"https://doi.org/10.1093/ismejo/wrae209","url":null,"abstract":"Quickly after birth, the gut microbiota is shaped via species acquisition and resource pressure. Breastmilk, and more specifically, human milk oligosaccharides are a determining factor in the formation of microbial communities and the interactions between bacteria. Prominent human milk oligosaccharide degraders have been rigorously characterized, but it is not known how the gut microbiota is shaped as a complex community. Here, we designed BIG-Syc, a synthetic community of 13 strains from the gut of vaginally born, breastfed infants. BIG-Syc replicated key compositional, metabolic, and proteomic characteristics of the gut microbiota of infants. Upon fermentation of a 4 and 5 human milk oligosaccharide mix, BIG-Syc demonstrated different compositional and proteomic profiles, with Bifidobacterium infantis and Bifidobacterium bifidum suppressing one another. The mix of 5 human milk oligosaccharides resulted in a more diverse composition with dominance of B. bifidum, whereas that with 4 human milk oligosaccharides supported the dominance of B. infantis, in 4 of 6 replicates. Reintroduction of bifidobacteria to BIG-Syc led to their engraftment and establishment of their niche. Based on proteomics and genome-scale metabolic models, we reconstructed the carbon source utilization and metabolite and gas production per strain. BIG-Syc demonstrated teamwork as cross-feeders utilized simpler carbohydrates, organic acids, and gases released from human milk oligosaccharide degraders. Collectively, our results showed that human milk oligosaccharides prompt resource-sharing for their complete degradation while leading to a different compositional and functional profile in the community. At the same time, BIG-Syc proved to be an accurate model for the representation of intra-microbe interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"29 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142449619","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}
Jule Freudenthal, Kenneth Dumack, Stefan Schaffer, Martin Schlegel, Michael Bonkowski
With over 3 trillion trees, forest ecosystems comprise nearly one-third of the terrestrial surface of the Earth. Very little attention has been given to the exploration of the above-ground plant microbiome of trees, its complex trophic interactions, and variations among tree species. To address this knowledge gap, we applied a primer-independent shotgun metatranscriptomic approach to assess the entire living canopy bark microbiome comprising prokaryotic and eukaryotic primary producers, decomposers, and various groups of consumers. With almost 1500 genera, we found a high microbial diversity on three tree species with distinct bark textures: oak (Quercus robur), linden (Tilia cordata), both with rough bark, and maple (Acer pseudoplatanus) with smooth bark. Core co-occurrence network analysis revealed a rich food web dominated by algal primary producers, and bacterial and fungal decomposers, sustaining a diverse community of consumers, including protists, microscopic metazoans and predatory bacteria. Whereas maple accommodated a depauperate microbiome, oak and linden accommodated a richer microbiome mainly differing in their relative community composition: Bacteria exhibited an increased dominance on linden, whereas co-occurring algae and fungi dominated on oak, highlighting the importance of algal-fungal lichen symbioses even at the microscopic scale. Further, due to bacteria-fungi co-exclusion, bacteria on bark are not the main beneficiaries of algae-derived carbon compounds as it is known from aquatic systems.
{"title":"Algae-fungi symbioses and bacteria-fungi co-exclusion drive tree species-specific differences in canopy bark microbiomes","authors":"Jule Freudenthal, Kenneth Dumack, Stefan Schaffer, Martin Schlegel, Michael Bonkowski","doi":"10.1093/ismejo/wrae206","DOIUrl":"https://doi.org/10.1093/ismejo/wrae206","url":null,"abstract":"With over 3 trillion trees, forest ecosystems comprise nearly one-third of the terrestrial surface of the Earth. Very little attention has been given to the exploration of the above-ground plant microbiome of trees, its complex trophic interactions, and variations among tree species. To address this knowledge gap, we applied a primer-independent shotgun metatranscriptomic approach to assess the entire living canopy bark microbiome comprising prokaryotic and eukaryotic primary producers, decomposers, and various groups of consumers. With almost 1500 genera, we found a high microbial diversity on three tree species with distinct bark textures: oak (Quercus robur), linden (Tilia cordata), both with rough bark, and maple (Acer pseudoplatanus) with smooth bark. Core co-occurrence network analysis revealed a rich food web dominated by algal primary producers, and bacterial and fungal decomposers, sustaining a diverse community of consumers, including protists, microscopic metazoans and predatory bacteria. Whereas maple accommodated a depauperate microbiome, oak and linden accommodated a richer microbiome mainly differing in their relative community composition: Bacteria exhibited an increased dominance on linden, whereas co-occurring algae and fungi dominated on oak, highlighting the importance of algal-fungal lichen symbioses even at the microscopic scale. Further, due to bacteria-fungi co-exclusion, bacteria on bark are not the main beneficiaries of algae-derived carbon compounds as it is known from aquatic systems.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"124 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142448353","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}
Autotrophic antimony (Sb) oxidation coupled to nitrate reduction plays an important role in the transformation and detoxification of Sb. However, the specific oxidase involved in this process has yet to be identified. Herein, we enriched the microbiota capable of nitrate-dependent Sb(III) oxidation and identified a new Sb(III) oxidase in an uncultured member of Symbiobacteriaceae. Incubation experiments demonstrated that nitrate-dependent Sb(III) oxidation occurred in the microcosm supplemented with Sb(III) and nitrate. Both the 16S rRNA gene and metagenomic analyses indicated that a species within Symbiobacteriaceae played a crucial role in this process. Furthermore, carbon-13 isotope labelling with carbon dioxide-fixing Rhodopseudomonas palustris in combination with nanoscale secondary ion mass spectrometry revealed that a newly characterized oxidase from the dimethylsulfoxide reductase family, designated as NaoABC, was responsible for autotrophic Sb(III) oxidation coupled with nitrate reduction. The NaoABC complex functions in conjunction with the nitrate reductase NarGHI, forming a redox loop that transfers electrons from Sb(III) to nitrate, thereby generating the energy necessary for autotrophic growth. This research offers new insights into the understanding of how microbes link Sb and nitrogen biogeochemical cycles in the environment.
{"title":"Nitrate-dependent antimony oxidase in an uncultured Symbiobacteriaceae member","authors":"Liying Wang, Zhipeng Yin, Wei Yan, Jialong Hao, Fei Tian, Jianbo Shi","doi":"10.1093/ismejo/wrae204","DOIUrl":"https://doi.org/10.1093/ismejo/wrae204","url":null,"abstract":"Autotrophic antimony (Sb) oxidation coupled to nitrate reduction plays an important role in the transformation and detoxification of Sb. However, the specific oxidase involved in this process has yet to be identified. Herein, we enriched the microbiota capable of nitrate-dependent Sb(III) oxidation and identified a new Sb(III) oxidase in an uncultured member of Symbiobacteriaceae. Incubation experiments demonstrated that nitrate-dependent Sb(III) oxidation occurred in the microcosm supplemented with Sb(III) and nitrate. Both the 16S rRNA gene and metagenomic analyses indicated that a species within Symbiobacteriaceae played a crucial role in this process. Furthermore, carbon-13 isotope labelling with carbon dioxide-fixing Rhodopseudomonas palustris in combination with nanoscale secondary ion mass spectrometry revealed that a newly characterized oxidase from the dimethylsulfoxide reductase family, designated as NaoABC, was responsible for autotrophic Sb(III) oxidation coupled with nitrate reduction. The NaoABC complex functions in conjunction with the nitrate reductase NarGHI, forming a redox loop that transfers electrons from Sb(III) to nitrate, thereby generating the energy necessary for autotrophic growth. This research offers new insights into the understanding of how microbes link Sb and nitrogen biogeochemical cycles in the environment.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"29 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142444255","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}
Chemolithoautotrophic nitrifiers are model groups for linking phylogeny, evolution, and ecophysiology. Ammonia-oxidising bacteria (AOB) typically dominate the first step of ammonia oxidation at high ammonium supply rates, ammonia-oxidising archaea (AOA) and complete ammonia-oxidising Nitrospira (comammox) are often active at lower supply rates or during AOB inactivity, and nitrite-oxidising bacteria (NOB) complete canonical nitrification. Soil virus communities are dynamic but contributions to functional processes are largely undetermined. In addition, characterising viruses infecting hosts with low relative abundance, such as nitrifiers, may be constrained by vast viral diversity, partial genome recovery, and difficulties in host linkage. Here, we describe a targeted incubation study that aimed to determine whether growth of different nitrifier groups in soil is associated with active virus populations and if process-focussed analyses facilitate characterisation of high-quality virus genomes. dsDNA viruses infecting different nitrifier groups were enriched in situ via differential host inhibition. Growth of each nitrifier group was consistent with predicted inhibition profiles and concomitant with the abundance of their viruses. These included 61 high-quality/complete virus genomes 35-173 kb in length with minimal similarity to validated families. AOA viruses lacked ammonia monooxygenase sub-unit C (amoC) genes found in marine AOA viruses but some encoded AOA-specific multicopper oxidase type 1 (MCO1), previously implicated in copper acquisition, and suggesting a role in supporting energy metabolism of soil AOA. Findings demonstrate focussed incubation studies facilitate characterisation of active host-virus interactions associated with specific processes and viruses of soil AOA, AOB and NOB are dynamic and potentially influence nitrogen cycling processes.
{"title":"Activity of novel virus families infecting soil nitrifiers is concomitant with host niche differentiation","authors":"Sungeun Lee, Christina Hazard, Graeme W Nicol","doi":"10.1093/ismejo/wrae205","DOIUrl":"https://doi.org/10.1093/ismejo/wrae205","url":null,"abstract":"Chemolithoautotrophic nitrifiers are model groups for linking phylogeny, evolution, and ecophysiology. Ammonia-oxidising bacteria (AOB) typically dominate the first step of ammonia oxidation at high ammonium supply rates, ammonia-oxidising archaea (AOA) and complete ammonia-oxidising Nitrospira (comammox) are often active at lower supply rates or during AOB inactivity, and nitrite-oxidising bacteria (NOB) complete canonical nitrification. Soil virus communities are dynamic but contributions to functional processes are largely undetermined. In addition, characterising viruses infecting hosts with low relative abundance, such as nitrifiers, may be constrained by vast viral diversity, partial genome recovery, and difficulties in host linkage. Here, we describe a targeted incubation study that aimed to determine whether growth of different nitrifier groups in soil is associated with active virus populations and if process-focussed analyses facilitate characterisation of high-quality virus genomes. dsDNA viruses infecting different nitrifier groups were enriched in situ via differential host inhibition. Growth of each nitrifier group was consistent with predicted inhibition profiles and concomitant with the abundance of their viruses. These included 61 high-quality/complete virus genomes 35-173 kb in length with minimal similarity to validated families. AOA viruses lacked ammonia monooxygenase sub-unit C (amoC) genes found in marine AOA viruses but some encoded AOA-specific multicopper oxidase type 1 (MCO1), previously implicated in copper acquisition, and suggesting a role in supporting energy metabolism of soil AOA. Findings demonstrate focussed incubation studies facilitate characterisation of active host-virus interactions associated with specific processes and viruses of soil AOA, AOB and NOB are dynamic and potentially influence nitrogen cycling processes.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142444257","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}
Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton
Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.
{"title":"Gut microbiota carbon and sulfur metabolisms support Salmonella infections.","authors":"Ikaia Leleiwi,Katherine Kokkinias,Yongseok Kim,Maryam Baniasad,Michael Shaffer,Anice Sabag-Daigle,Rebecca A Daly,Rory M Flynn,Vicki H Wysocki,Brian M M Ahmer,Mikayla A Borton,Kelly C Wrighton","doi":"10.1093/ismejo/wrae187","DOIUrl":"https://doi.org/10.1093/ismejo/wrae187","url":null,"abstract":"Salmonella enterica serovar Typhimurium is a pervasive enteric pathogen and ongoing global threat to public health. Ecological studies in the Salmonella impacted gut remain underrepresented in the literature, discounting microbiome mediated interactions that may inform Salmonella physiology during colonization and infection. To understand the microbial ecology of Salmonella remodeling of the gut microbiome, we performed multi-omics on fecal microbial communities from untreated and Salmonella-infected mice. Reconstructed genomes recruited metatranscriptomic and metabolomic data providing a strain-resolved view of the expressed metabolisms of the microbiome during Salmonella infection. These data informed possible Salmonella interactions with members of the gut microbiome that were previously uncharacterized. Salmonella-induced inflammation significantly reduced the diversity of genomes that recruited transcripts in the gut microbiome, yet increased transcript mapping was observed for 7 members, among which Luxibacter and Ligilactobacillus transcript read recruitment was most prevalent. Metatranscriptomic insights from Salmonella and other persistent taxa in the inflamed microbiome further expounded the necessity for oxidative tolerance mechanisms to endure the host inflammatory responses to infection. In the inflamed gut lactate was a key metabolite, with microbiota production and consumption reported amongst members with detected transcript recruitment. We also showed that organic sulfur sources could be converted by gut microbiota to yield inorganic sulfur pools that become oxidized in the inflamed gut, resulting in thiosulfate and tetrathionate that supports Salmonella respiration. This research advances physiological microbiome insights beyond prior amplicon-based approaches, with the transcriptionally active organismal and metabolic pathways outlined here offering intriguing intervention targets in the Salmonella-infected intestine.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"193 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142439457","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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