Pub Date : 2025-09-19eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf161
Chyrene Moncada, Carol Arnosti, Jan D Brüwer, Dirk de Beer, Gunter Wegener, Peter Stief, Marit R van Erk, Jürgen Titschack, Rudolf Amann, Katrin Knittel
The remineralization of organic matter by benthic bacteria is an essential process in the marine carbon cycle. In polar regions, strong variation in daylength causes pronounced seasonality in primary productivity, but the responses of sedimentary bacteria to these fluctuations are not well understood. We investigated the seasonal dynamics of benthic bacterial communities from an Arctic fjord and found a partitioning of the communities into seasonally responsive and stable guilds. We separately analyzed the fractions of cells in the porewater and those loosely and firmly attached to sand grains through 16S ribosomal RNA gene sequencing, cell counting, rate measurements, and geochemical analyses. The porewater and loosely attached bacterial communities showed a dynamic response in composition and activity, suggesting that they play a central role in benthic-pelagic coupling by responding rapidly to seasonal fluctuations in organic matter availability. In contrast, the majority of the firmly attached cells showed a more buffered response, as reflected, e.g. in the consistently high cell numbers of Woeseiaceae. This fraction is potentially key to maintaining baseline remineralization processes throughout the year, independent of fresh organic matter input. These findings provide a new mechanistic understanding of carbon cycling in Arctic surface sediments that may also apply beyond polar regions.
{"title":"Seasonal and stable heterotrophic guilds drive Arctic benthic microbiome functioning across polar day and night.","authors":"Chyrene Moncada, Carol Arnosti, Jan D Brüwer, Dirk de Beer, Gunter Wegener, Peter Stief, Marit R van Erk, Jürgen Titschack, Rudolf Amann, Katrin Knittel","doi":"10.1093/ismeco/ycaf161","DOIUrl":"10.1093/ismeco/ycaf161","url":null,"abstract":"<p><p>The remineralization of organic matter by benthic bacteria is an essential process in the marine carbon cycle. In polar regions, strong variation in daylength causes pronounced seasonality in primary productivity, but the responses of sedimentary bacteria to these fluctuations are not well understood. We investigated the seasonal dynamics of benthic bacterial communities from an Arctic fjord and found a partitioning of the communities into seasonally responsive and stable guilds. We separately analyzed the fractions of cells in the porewater and those loosely and firmly attached to sand grains through 16S ribosomal RNA gene sequencing, cell counting, rate measurements, and geochemical analyses. The porewater and loosely attached bacterial communities showed a dynamic response in composition and activity, suggesting that they play a central role in benthic-pelagic coupling by responding rapidly to seasonal fluctuations in organic matter availability. In contrast, the majority of the firmly attached cells showed a more buffered response, as reflected, e.g. in the consistently high cell numbers of <i>Woeseiaceae</i>. This fraction is potentially key to maintaining baseline remineralization processes throughout the year, independent of fresh organic matter input. These findings provide a new mechanistic understanding of carbon cycling in Arctic surface sediments that may also apply beyond polar regions.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf161"},"PeriodicalIF":6.1,"publicationDate":"2025-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12503162/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145253945","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-19eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf165
Shunan Zhao, Fangzhou Wang, Liuying Song, Shaoqing Zhu, Suo Liu, Kai Zhao, Ruiping Liu, Yu-You Li
Robust interspecies interactions are essential for efficient methanogenesis in anaerobic digestion. This study investigated the impact of quorum sensing (QS) enhancement on the succession of methanogenic communities during anaerobic digestion. The QS stimulation via exogenous N-acyl-homoserine lactones enhanced methane production by 18.8%-22.1%. Moreover, QS shaped microbial community succession toward a more deterministic assembly, selectively enriching key syntrophs (Pelotomaculum, Smithella), and methanogens (Methanobacterium, Methanothrix). Metagenomic analysis revealed that QS induced genes related to transcription, transport, and cofactor biosynthesis instead of directly regulating carbon metabolism. In this context, interspecies electron transfer emerges as a critical factor regulating interspecies interactions under QS regulation. Specifically, QS enhancement boosted redox mediator secretion, and the concentration of 2-amino-3-carboxy-1,4-naphthoquinone and phenazine increased by 7.8- and 4.8-fold, respectively. QS enhancement also induced higher abundance of c-type cytochromes. Moreover, the higher electron transfer coefficients were detected with 40.2%-89.9% increase. Further, QS also enhanced relative abundance of genes involved in Complex I/III and ferredoxin-dependent hydrogenases, promoting electron flow from syntrophs to methanogens. These effects induced higher relative abundance of genes associated with syntrophic propionate/butyrate oxidation and hydrogenotrophic/acetotrophic methanogenesis. Collectively, given that the similar regulation pathway is widely distributed in anaerobes, these findings identify QS as a critical ecological signal that drives functional microbial succession.
{"title":"Interspecies electron transfer as one of key drivers of methanogenic consortia succession within quorum sensing regulation.","authors":"Shunan Zhao, Fangzhou Wang, Liuying Song, Shaoqing Zhu, Suo Liu, Kai Zhao, Ruiping Liu, Yu-You Li","doi":"10.1093/ismeco/ycaf165","DOIUrl":"10.1093/ismeco/ycaf165","url":null,"abstract":"<p><p>Robust interspecies interactions are essential for efficient methanogenesis in anaerobic digestion. This study investigated the impact of quorum sensing (QS) enhancement on the succession of methanogenic communities during anaerobic digestion. The QS stimulation via exogenous N-acyl-homoserine lactones enhanced methane production by 18.8%-22.1%. Moreover, QS shaped microbial community succession toward a more deterministic assembly, selectively enriching key syntrophs (<i>Pelotomaculum</i>, <i>Smithella</i>), and methanogens (<i>Methanobacterium</i>, <i>Methanothrix</i>). Metagenomic analysis revealed that QS induced genes related to transcription, transport, and cofactor biosynthesis instead of directly regulating carbon metabolism. In this context, interspecies electron transfer emerges as a critical factor regulating interspecies interactions under QS regulation. Specifically, QS enhancement boosted redox mediator secretion, and the concentration of 2-amino-3-carboxy-1,4-naphthoquinone and phenazine increased by 7.8- and 4.8-fold, respectively. QS enhancement also induced higher abundance of c-type cytochromes. Moreover, the higher electron transfer coefficients were detected with 40.2%-89.9% increase. Further, QS also enhanced relative abundance of genes involved in Complex I/III and ferredoxin-dependent hydrogenases, promoting electron flow from syntrophs to methanogens. These effects induced higher relative abundance of genes associated with syntrophic propionate/butyrate oxidation and hydrogenotrophic/acetotrophic methanogenesis. Collectively, given that the similar regulation pathway is widely distributed in anaerobes, these findings identify QS as a critical ecological signal that drives functional microbial succession.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf165"},"PeriodicalIF":6.1,"publicationDate":"2025-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12503159/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145253950","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Successional pathways of microbial communities are influenced by the complex interactive dynamics among the resident and immigrating species, along with the interactive feedback loops with their environment. Although studies on microbial communities have described patterns of microbial succession, quantitative evidence of how resident communities respond to immigrating species and how such relationships translate into successional changes remains limited, especially for species-rich communities under natural settings. Here, we carried out a field experiment to investigate how the identity of immigrating species influences the successional pathways of wood-inhabiting fungi. We simulated immigration through inoculations of nine selected wood-inhabiting fungal species and characterized resident fungal communities before and one and two years after the inoculations through DNA metabarcoding. The experiments included 275 naturally fallen and 185 artificially felled fresh logs of Norway spruce, with different log types hosting distinct initial resident communities of fungi and representing different abiotic conditions. While the resident community succession was mostly explained by the log-level abiotic characteristics, the identity of immigrating species also influenced the composition of resident communities, and consequently community succession. The immigrating species influenced resident species mostly negatively, suggesting competitive interactions to be important determinants of community succession. The responses of resident species to the immigrating species were phylogenetically correlated, suggesting that shared traits underlie species interactions in the species-rich wood-inhabiting fungal communities. This study advanced the understanding of community succession in species-rich natural systems by providing experimental evidence that the immigrating species influence community succession through the phylogenetically structured responses of resident species.
{"title":"Experimental species introductions influence fungal community succession through positive and negative effects on resident species.","authors":"Sonja Saine, Tadashi Fukami, Reijo Penttilä, Brendan Furneaux, Otso Ovaskainen, Nerea Abrego","doi":"10.1093/ismeco/ycaf166","DOIUrl":"10.1093/ismeco/ycaf166","url":null,"abstract":"<p><p>Successional pathways of microbial communities are influenced by the complex interactive dynamics among the resident and immigrating species, along with the interactive feedback loops with their environment. Although studies on microbial communities have described patterns of microbial succession, quantitative evidence of how resident communities respond to immigrating species and how such relationships translate into successional changes remains limited, especially for species-rich communities under natural settings. Here, we carried out a field experiment to investigate how the identity of immigrating species influences the successional pathways of wood-inhabiting fungi. We simulated immigration through inoculations of nine selected wood-inhabiting fungal species and characterized resident fungal communities before and one and two years after the inoculations through DNA metabarcoding. The experiments included 275 naturally fallen and 185 artificially felled fresh logs of Norway spruce, with different log types hosting distinct initial resident communities of fungi and representing different abiotic conditions. While the resident community succession was mostly explained by the log-level abiotic characteristics, the identity of immigrating species also influenced the composition of resident communities, and consequently community succession. The immigrating species influenced resident species mostly negatively, suggesting competitive interactions to be important determinants of community succession. The responses of resident species to the immigrating species were phylogenetically correlated, suggesting that shared traits underlie species interactions in the species-rich wood-inhabiting fungal communities. This study advanced the understanding of community succession in species-rich natural systems by providing experimental evidence that the immigrating species influence community succession through the phylogenetically structured responses of resident species.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf166"},"PeriodicalIF":6.1,"publicationDate":"2025-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12510464/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145282117","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-17eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf163
Loudon Herold, Bradley G Fitzgerald, Gwenno M E Leclercq, Matthew T Sorbara
Nutrient niche access by the gut microbiota impacts community assembly and dynamics, the production of host-benefiting short-chain fatty acids (SCFAs), and pathogen inhibition through colonization resistance. Furthermore, deciphering if and how niche access varies on a strain level will be important as individual strains of gut microbes are selected for inclusion in new live biotherapeutic products. Despite this, for many gut anaerobes, nutrient niche occupancy and impacts of strain variation remain unknown. Here, we examined nutrient niches of Anaerostipes hadrus (AH), a butyrate-producing member of the Lachnospiraceae family. We found that AH isolates encode a carbohydrate metabolism gene repertoire that is distinct from other Lachnospiraceae. Furthermore, tested AH isolates show variation in carbohydrate-related genes between strains and large numbers of genes associated with horizontal gene transfer events. Functionally, we demonstrate that AH isolates exhibit strain-specific patterns of nutrient niche access that can be associated with the gain, loss, and disruption of gene clusters enabling specific carbohydrate metabolism. This strain-specific carbohydrate use drives variable SCFA production. Unexpectedly, strains exhibit differential preferences for carbohydrates, which alter SCFA profiles in environments with multiple possible nutrient niches available. Furthermore, when strains of AH interact in an environment with multiple nutrient niches available, strain-strain interactions result in varying SCFA profiles that extend beyond the additive effects of individual strain behavior. Altogether, these results demonstrate the importance of evaluating strain-level variation in the design of future live biotherapeutic products.
{"title":"Strain-level variation controls nutrient niche occupancy by health-associated <i>Anaerostipes hadrus</i>.","authors":"Loudon Herold, Bradley G Fitzgerald, Gwenno M E Leclercq, Matthew T Sorbara","doi":"10.1093/ismeco/ycaf163","DOIUrl":"10.1093/ismeco/ycaf163","url":null,"abstract":"<p><p>Nutrient niche access by the gut microbiota impacts community assembly and dynamics, the production of host-benefiting short-chain fatty acids (SCFAs), and pathogen inhibition through colonization resistance. Furthermore, deciphering if and how niche access varies on a strain level will be important as individual strains of gut microbes are selected for inclusion in new live biotherapeutic products. Despite this, for many gut anaerobes, nutrient niche occupancy and impacts of strain variation remain unknown. Here, we examined nutrient niches of <i>Anaerostipes hadrus</i> (AH)<i>,</i> a butyrate-producing member of the <i>Lachnospiraceae</i> family. We found that AH isolates encode a carbohydrate metabolism gene repertoire that is distinct from other <i>Lachnospiraceae</i>. Furthermore, tested AH isolates show variation in carbohydrate-related genes between strains and large numbers of genes associated with horizontal gene transfer events. Functionally, we demonstrate that AH isolates exhibit strain-specific patterns of nutrient niche access that can be associated with the gain, loss, and disruption of gene clusters enabling specific carbohydrate metabolism. This strain-specific carbohydrate use drives variable SCFA production. Unexpectedly, strains exhibit differential preferences for carbohydrates, which alter SCFA profiles in environments with multiple possible nutrient niches available. Furthermore, when strains of AH interact in an environment with multiple nutrient niches available, strain-strain interactions result in varying SCFA profiles that extend beyond the additive effects of individual strain behavior. Altogether, these results demonstrate the importance of evaluating strain-level variation in the design of future live biotherapeutic products.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf163"},"PeriodicalIF":6.1,"publicationDate":"2025-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12503163/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145253939","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-17eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf164
Ruixian Sun, Wenqian Xu, Yangbing Xu, Zhimeng Xu, Yehui Tan, Jiying Li, Hongbin Liu, Charmaine C M Yung
Marine viruses play critical roles in shaping microbial communities and driving biogeochemical cycles, yet their dynamics in estuarine systems are not well characterized. Here, we conducted a comprehensive metagenomic analysis of viral communities and virus-host interactions across the Pearl River estuary, a dynamic subtropical estuary in southern China. Using 24 metagenomic libraries from eight sampling sites, we identified 29,952 viral populations, with Uroviricota and potential Uroviricota accounted for 80.48% of taxa, underscoring their ecological importance. A key finding of our integrated analysis is the unexpectedly high abundance of nucleocytoplasmic large DNA viruses in offshore waters, which suggests a more significant role for eukaryotic viruses in coastal ecosystems than previously acknowledged and correlates with elevated levels of their eukaryotic hosts. Environmental variables, particularly salinity and nutrient availability, emerged as key drivers of viral and host distribution patterns. By linking environmental gradients to distinct community "envirotypes" and their underlying genomic features, we revealed novel virus-host interactions and highlighted the impact of environmental gradients on microbial ecology. Additionally, viral auxiliary metabolic genes linked to phosphorus and nitrogen metabolism suggest critical roles in modulating host metabolic pathways and influencing nutrient cycling. Our findings demonstrate how spatial heterogeneity and environmental gradients shape viral and microbial ecology in estuarine ecosystems. Our findings provide a holistic, multi-domain view of microbial and viral ecology, demonstrating how integrating prokaryotic, eukaryotic, and viral community analyses offers a more complete understanding of ecosystem function in these critical transition zones.
{"title":"Environmental gradients shape viral-host dynamics in the Pearl River estuary.","authors":"Ruixian Sun, Wenqian Xu, Yangbing Xu, Zhimeng Xu, Yehui Tan, Jiying Li, Hongbin Liu, Charmaine C M Yung","doi":"10.1093/ismeco/ycaf164","DOIUrl":"10.1093/ismeco/ycaf164","url":null,"abstract":"<p><p>Marine viruses play critical roles in shaping microbial communities and driving biogeochemical cycles, yet their dynamics in estuarine systems are not well characterized. Here, we conducted a comprehensive metagenomic analysis of viral communities and virus-host interactions across the Pearl River estuary, a dynamic subtropical estuary in southern China. Using 24 metagenomic libraries from eight sampling sites, we identified 29,952 viral populations, with Uroviricota and potential Uroviricota accounted for 80.48% of taxa, underscoring their ecological importance. A key finding of our integrated analysis is the unexpectedly high abundance of nucleocytoplasmic large DNA viruses in offshore waters, which suggests a more significant role for eukaryotic viruses in coastal ecosystems than previously acknowledged and correlates with elevated levels of their eukaryotic hosts. Environmental variables, particularly salinity and nutrient availability, emerged as key drivers of viral and host distribution patterns. By linking environmental gradients to distinct community \"envirotypes\" and their underlying genomic features, we revealed novel virus-host interactions and highlighted the impact of environmental gradients on microbial ecology. Additionally, viral auxiliary metabolic genes linked to phosphorus and nitrogen metabolism suggest critical roles in modulating host metabolic pathways and influencing nutrient cycling. Our findings demonstrate how spatial heterogeneity and environmental gradients shape viral and microbial ecology in estuarine ecosystems. Our findings provide a holistic, multi-domain view of microbial and viral ecology, demonstrating how integrating prokaryotic, eukaryotic, and viral community analyses offers a more complete understanding of ecosystem function in these critical transition zones.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf164"},"PeriodicalIF":6.1,"publicationDate":"2025-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12533691/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145330940","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-16eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf162
Karoline Jetter, Kunal Jani, Kerstin Wilhelm, Ulrike Stehle, Rostand R Chamedjeu, Christian U Riedel, Lena Wilfert, Patrick Schäfer, Simone Sommer
Agricultural grasslands are often managed intensively, influencing soil properties and microbial communities. These changes may, in turn, affect the microbiome of organisms across multiple trophic levels within the same habitat, and significant shifts in these communities can disrupt health and functionality along the entire trophic chain. This study investigates how fertilization affects microbial communities in multiple connected below- and above-ground trophic compartments of grassland ecosystems. We compared control grassland sites to those treated with organic fertilizers-biogas digestate, cow/horse manure, and pig slurry-using 16S rRNA amplicon sequencing and soil nutrient analysis. Shifts in microbial composition occurred in response to fertilization, with compartment-dependent effects. Changes were more pronounced in belowground compartments, with pig slurry fertilization exhibiting the most substantial impact. Overlapping bacterial genera detected among soil, roots, and higher trophic levels show the potential strong interactions across trophic levels shaping microbial communities. Pig slurry-derived microbial taxa were found in all compartments, but their low prevalence suggests an indirect effect of fertilization, primarily due to changes in nutrient availability. Compared to the control sites, pig slurry-fertilized sites showed proliferation of certain taxa, including Clostridium, Ruminococcus or Lachnoclostridium, particularly in the animal compartments. Our study highlights that the effects of fertilization permeate all trophic levels, with potential ecological and health implications aligned with the One Health framework.
{"title":"Fertilization impacts microbiomes along the grassland trophic chain.","authors":"Karoline Jetter, Kunal Jani, Kerstin Wilhelm, Ulrike Stehle, Rostand R Chamedjeu, Christian U Riedel, Lena Wilfert, Patrick Schäfer, Simone Sommer","doi":"10.1093/ismeco/ycaf162","DOIUrl":"10.1093/ismeco/ycaf162","url":null,"abstract":"<p><p>Agricultural grasslands are often managed intensively, influencing soil properties and microbial communities. These changes may, in turn, affect the microbiome of organisms across multiple trophic levels within the same habitat, and significant shifts in these communities can disrupt health and functionality along the entire trophic chain. This study investigates how fertilization affects microbial communities in multiple connected below- and above-ground trophic compartments of grassland ecosystems. We compared control grassland sites to those treated with organic fertilizers-biogas digestate, cow/horse manure, and pig slurry-using 16S rRNA amplicon sequencing and soil nutrient analysis. Shifts in microbial composition occurred in response to fertilization, with compartment-dependent effects. Changes were more pronounced in belowground compartments, with pig slurry fertilization exhibiting the most substantial impact. Overlapping bacterial genera detected among soil, roots, and higher trophic levels show the potential strong interactions across trophic levels shaping microbial communities. Pig slurry-derived microbial taxa were found in all compartments, but their low prevalence suggests an indirect effect of fertilization, primarily due to changes in nutrient availability. Compared to the control sites, pig slurry-fertilized sites showed proliferation of certain taxa, including <i>Clostridium, Ruminococcus</i> or <i>Lachnoclostridium</i>, particularly in the animal compartments. Our study highlights that the effects of fertilization permeate all trophic levels, with potential ecological and health implications aligned with the One Health framework.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf162"},"PeriodicalIF":6.1,"publicationDate":"2025-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12503161/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145253979","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-16eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf153
Gaspard Rihm, Fabio Benedetti, Lucie Bittner
Marine unicellular eukaryotes (protists) exhibit a wide spectrum of trophic strategies ranging from specialists (strict phototrophy or strict phagotrophy) to generalist (mixotrophy). Generalist strategies enable flexibility in nutrient sources, which impacts biogeochemical cycles, energy fluxes in planktonic food webs as well as species biogeography. Dinoflagellates exhibit specialist and generalist trophic strategies, making them a key group for studying the ecological success of trophic traits from a biogeographical perspective. Yet, our understanding of what drives their biogeography remains limited although they are a major component of planktonic communities. Here, we combine one of the largest environmental genomics databases with state-of-the-art species distribution modelling to test whether trophic dinoflagellate specialists exhibit distinct spatial distributions and abiotic drivers compared to generalists. Based on field observations alone, we find that dinoflagellate species show similar abundance and evenness patterns, regardless of their trophic strategies. However, our models reveal differences in environmental niches at the trait level: mixotrophy is favoured in tropical oligotrophic regions whereas strict phagotrophy is favoured in the productive high-latitudes. At the species level, mixotrophs show similar responses across gradients of nutrient availability, whereas species responses to abiotic gradients are more divergent within strict phagotrophs. The latter pattern is consistent with a trait scenario of multiple evolutionary convergences. We show that trophic classification effectively explains the distribution patterns and environmental responses of generalists but is less effective in capturing the diverse responses of specialists that could result from other factors (evolutionary history, biotic interactions, cell size).
{"title":"Do trophic strategies shape biogeography and environmental niches? Marine dinoflagellates as a case study.","authors":"Gaspard Rihm, Fabio Benedetti, Lucie Bittner","doi":"10.1093/ismeco/ycaf153","DOIUrl":"10.1093/ismeco/ycaf153","url":null,"abstract":"<p><p>Marine unicellular eukaryotes (protists) exhibit a wide spectrum of trophic strategies ranging from specialists (strict phototrophy or strict phagotrophy) to generalist (mixotrophy). Generalist strategies enable flexibility in nutrient sources, which impacts biogeochemical cycles, energy fluxes in planktonic food webs as well as species biogeography. Dinoflagellates exhibit specialist and generalist trophic strategies, making them a key group for studying the ecological success of trophic traits from a biogeographical perspective. Yet, our understanding of what drives their biogeography remains limited although they are a major component of planktonic communities. Here, we combine one of the largest environmental genomics databases with state-of-the-art species distribution modelling to test whether trophic dinoflagellate specialists exhibit distinct spatial distributions and abiotic drivers compared to generalists. Based on field observations alone, we find that dinoflagellate species show similar abundance and evenness patterns, regardless of their trophic strategies. However, our models reveal differences in environmental niches at the trait level: mixotrophy is favoured in tropical oligotrophic regions whereas strict phagotrophy is favoured in the productive high-latitudes. At the species level, mixotrophs show similar responses across gradients of nutrient availability, whereas species responses to abiotic gradients are more divergent within strict phagotrophs. The latter pattern is consistent with a trait scenario of multiple evolutionary convergences. We show that trophic classification effectively explains the distribution patterns and environmental responses of generalists but is less effective in capturing the diverse responses of specialists that could result from other factors (evolutionary history, biotic interactions, cell size).</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf153"},"PeriodicalIF":6.1,"publicationDate":"2025-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12452278/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145132812","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-15eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf159
Kendra Turk-Kubo, Mar Benavides, Matthew M Mills, Sarah R Smith
Some Rhizosolenia diatoms living in oligotrophic marine ecosystems are known to form large, conspicuous mats and are thought to be sources of new nitrogen to surface waters via vertical migration to the nitracline where subsurface nitrate is accessed for growth. These vertically migrating Rhizosolenia mats are chronically under sampled, and both the diatom species comprising the mats and the associated microbiome have not been characterized using modern molecular techniques. Here we present the first DNA-based analysis of Rhizosolenia mats collected in the North Pacific Subtropical Gyre. Using sequencing of 18S rRNA and nifH genes (a proxy for N2 fixation capacity), we report on the molecular diversity of mat-forming Rhizosolenia species, which include two newly sequenced clades, and an assemblage of associated N2-fixing microorganisms that is distinct from the non-mat associated water column assemblage. Our findings advance knowledge of oligotrophic diatom diversity and challenge prevailing views of their nitrogen sources, suggesting these mats may obtain nitrogen through association-based N2 fixation. Further work is needed to understand the nature of these associations, and whether Rhizosolenia mat communities are a significant unrecognized source of N2-fixation-derived new nitrogen to the oligotrophic surface waters.
{"title":"<i>Rhizosolenia</i> mat diatoms associate with nitrogen-fixing microbes.","authors":"Kendra Turk-Kubo, Mar Benavides, Matthew M Mills, Sarah R Smith","doi":"10.1093/ismeco/ycaf159","DOIUrl":"10.1093/ismeco/ycaf159","url":null,"abstract":"<p><p>Some <i>Rhizosolenia</i> diatoms living in oligotrophic marine ecosystems are known to form large, conspicuous mats and are thought to be sources of new nitrogen to surface waters via vertical migration to the nitracline where subsurface nitrate is accessed for growth. These vertically migrating <i>Rhizosolenia</i> mats are chronically under sampled, and both the diatom species comprising the mats and the associated microbiome have not been characterized using modern molecular techniques. Here we present the first DNA-based analysis of <i>Rhizosolenia</i> mats collected in the North Pacific Subtropical Gyre. Using sequencing of 18S rRNA and <i>nifH</i> genes (a proxy for N<sub>2</sub> fixation capacity), we report on the molecular diversity of mat-forming <i>Rhizosolenia</i> species, which include two newly sequenced clades, and an assemblage of associated N<sub>2</sub>-fixing microorganisms that is distinct from the non-mat associated water column assemblage. Our findings advance knowledge of oligotrophic diatom diversity and challenge prevailing views of their nitrogen sources, suggesting these mats may obtain nitrogen through association-based N<sub>2</sub> fixation. Further work is needed to understand the nature of these associations, and whether <i>Rhizosolenia</i> mat communities are a significant unrecognized source of N<sub>2</sub>-fixation-derived new nitrogen to the oligotrophic surface waters.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf159"},"PeriodicalIF":6.1,"publicationDate":"2025-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12499774/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145245947","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-11eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf160
Małgorzata M Lipowska, Edyta T Sadowska, Kevin D Kohl, Paweł Koteja
According to the "hologenome" theory of evolution, natural selection and evolution can act through a conglomerate biological unit, the "holobiont"-the host and its associated microbiome. Although the concept is appealing and emerges as a unifying paradigm, its merits are debated, and few attempts have been made to directly test its specific assumptions using the approaches of experimental evolution. Here, we fill this gap using a unique model system: lines of bank vole (Clethrionomys = Myodes glareolus) selected for enhanced ability to grow or maintain body mass in 4-day test with a low-quality herbivorous diet and unselected control lines. Results from a complex nature-nurture design, in which we combined the selection experiment with dietary treatment and cohabitation between individuals from the distinct lines (to allow for horizontal bacterial transfer), showed that the "herbivorous" voles harbored a cecal microbiome community with altered membership and structure, and altered abundances of several phyla and genera, regardless of the origin of the cohabitant. Although the differences were small, they were statistically significant and partially robust to changes in diet and housing conditions. Microbial characteristics also correlated with host selection-related performance traits at the level of individual variation. These results, combined with those of a complementary cross-fostering experiment, showed that under these contexts, the microbiome is largely determined by genetic background (effect of selection) and early maternal effects, and can be altered in response to selection acting on other organismal traits. Such results are consistent with assumptions underlying the concept of hologenomic evolution.
{"title":"Experimental evolution of a mammalian holobiont: bank voles selected for herbivorous capability evolved distinct and robust gut bacterial communities.","authors":"Małgorzata M Lipowska, Edyta T Sadowska, Kevin D Kohl, Paweł Koteja","doi":"10.1093/ismeco/ycaf160","DOIUrl":"10.1093/ismeco/ycaf160","url":null,"abstract":"<p><p>According to the \"hologenome\" theory of evolution, natural selection and evolution can act through a conglomerate biological unit, the \"holobiont\"-the host and its associated microbiome. Although the concept is appealing and emerges as a unifying paradigm, its merits are debated, and few attempts have been made to directly test its specific assumptions using the approaches of experimental evolution. Here, we fill this gap using a unique model system: lines of bank vole (<i>Clethrionomys = Myodes glareolus</i>) selected for enhanced ability to grow or maintain body mass in 4-day test with a low-quality herbivorous diet and unselected control lines. Results from a complex nature-nurture design, in which we combined the selection experiment with dietary treatment and cohabitation between individuals from the distinct lines (to allow for horizontal bacterial transfer), showed that the \"herbivorous\" voles harbored a cecal microbiome community with altered membership and structure, and altered abundances of several phyla and genera, regardless of the origin of the cohabitant. Although the differences were small, they were statistically significant and partially robust to changes in diet and housing conditions. Microbial characteristics also correlated with host selection-related performance traits at the level of individual variation. These results, combined with those of a complementary cross-fostering experiment, showed that under these contexts, the microbiome is largely determined by genetic background (effect of selection) and early maternal effects, and can be altered in response to selection acting on other organismal traits. Such results are consistent with assumptions underlying the concept of hologenomic evolution.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf160"},"PeriodicalIF":6.1,"publicationDate":"2025-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12516954/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145294703","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-10eCollection Date: 2025-01-01DOI: 10.1093/ismeco/ycaf140
Borja Aldeguer-Riquelme, Luis M Rodriguez-R, Konstantinos T Konstantinidis
The importance of rarefying ecological or amplicon sequencing data to a standardized level of diversity coverage for reliable diversity comparisons across samples is well recognized. However, the importance of diversity coverage, i.e. the fraction of the genomic diversity of a sample sequenced, in comparative shotgun metagenomic studies remains frequently overlooked. Using both in silico and natural metagenomes from a wide range of environments, we demonstrate that uneven metagenome coverage can result in misleading biological conclusions, particularly for identifying differentially abundant features, i.e. groups of genes or genomes assigned to the same protein family or taxonomic rank, respectively, and for comparing diversity between samples. The main underlying cause is that not all members of a feature may be detectable, and thus counted, across such unevenly covered metagenomes depending on the sequencing effort applied and the underlying member-abundance curves. Unfortunately, 99.5% of previous comparative metagenomic studies have overlooked this metric, suggesting that their reported results might be misleading. We show that achieving high Nonpareil coverage (≥0.9), a metric that estimates metagenome diversity coverage, is the most reliable strategy to mitigate this issue. When high Nonpareil coverage is not achievable, such as for highly diverse and complex samples like soils, we show that standardizing (or subsampling) metagenomic datasets to the same Nonpareil coverage, rather than sequencing effort, prior to comparative analysis provides for more accurate results. We provide a set of practical recommendations and the corresponding Python scripts to help researchers to assess and standardize metagenome diversity coverage for their comparative analyses.
{"title":"Differences in metagenome coverage may confound abundance-based and diversity conclusions and how to deal with them.","authors":"Borja Aldeguer-Riquelme, Luis M Rodriguez-R, Konstantinos T Konstantinidis","doi":"10.1093/ismeco/ycaf140","DOIUrl":"10.1093/ismeco/ycaf140","url":null,"abstract":"<p><p>The importance of rarefying ecological or amplicon sequencing data to a standardized level of diversity coverage for reliable diversity comparisons across samples is well recognized. However, the importance of diversity coverage, i.e. the fraction of the genomic diversity of a sample sequenced, in comparative shotgun metagenomic studies remains frequently overlooked. Using both <i>in silico</i> and natural metagenomes from a wide range of environments, we demonstrate that uneven metagenome coverage can result in misleading biological conclusions, particularly for identifying differentially abundant features, i.e. groups of genes or genomes assigned to the same protein family or taxonomic rank, respectively, and for comparing diversity between samples. The main underlying cause is that not all members of a feature may be detectable, and thus counted, across such unevenly covered metagenomes depending on the sequencing effort applied and the underlying member-abundance curves. Unfortunately, 99.5% of previous comparative metagenomic studies have overlooked this metric, suggesting that their reported results might be misleading. We show that achieving high Nonpareil coverage (≥0.9), a metric that estimates metagenome diversity coverage, is the most reliable strategy to mitigate this issue. When high Nonpareil coverage is not achievable, such as for highly diverse and complex samples like soils, we show that standardizing (or subsampling) metagenomic datasets to the same Nonpareil coverage, rather than sequencing effort, prior to comparative analysis provides for more accurate results. We provide a set of practical recommendations and the corresponding Python scripts to help researchers to assess and standardize metagenome diversity coverage for their comparative analyses.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"5 1","pages":"ycaf140"},"PeriodicalIF":6.1,"publicationDate":"2025-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12477595/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145202184","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}