ISME communicationsPub Date : 2024-09-08eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae111
Raphael Eisenhofer, Antton Alberdi, Ben J Woodcroft
{"title":"Quantifying microbial DNA in metagenomes improves microbial trait estimation.","authors":"Raphael Eisenhofer, Antton Alberdi, Ben J Woodcroft","doi":"10.1093/ismeco/ycae111","DOIUrl":"https://doi.org/10.1093/ismeco/ycae111","url":null,"abstract":"<p><p>Shotgun metagenomics is a powerful tool for studying the genomic traits of microbial community members, such as genome size, gene content, etc. While such traits can be used to better understand the ecology and evolution of microbial communities, the accuracy of their estimations can be critically influenced by both known and unknown factors. One factor that can bias trait estimations is the proportion of eukaryotic and viral DNA in a metagenome, as some bioinformatic tools assume that all DNA reads in a metagenome are bacterial or archaeal. Here, we add to a recent debate about the influence of eukaryotic DNA in the estimation of average genome size from a global soil sample dataset using a new bioinformatic tool. Contrary to what was assumed, our reanalysis of this dataset revealed that soil samples can contain a substantial proportion of non-microbial DNA, which severely inflated the original estimates of average genome size. Correcting for this bias significantly improves the statistical support for the negative relationship between average bacterial genome size and soil pH. These results highlight that metagenomes can contain large quantities of non-microbial DNA and that new methods that correct for this can improve microbial trait estimation.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae111"},"PeriodicalIF":5.1,"publicationDate":"2024-09-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11439404/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333881","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}
ISME communicationsPub Date : 2024-09-04eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae107
Emma Bell, Jianwei Chen, William D L Richardson, Milovan Fustic, Casey R J Hubert
{"title":"Denitrification genotypes of endospore-forming <i>Bacillota</i>.","authors":"Emma Bell, Jianwei Chen, William D L Richardson, Milovan Fustic, Casey R J Hubert","doi":"10.1093/ismeco/ycae107","DOIUrl":"https://doi.org/10.1093/ismeco/ycae107","url":null,"abstract":"<p><p>Denitrification is a key metabolic process in the global nitrogen cycle and is performed by taxonomically diverse microorganisms. Despite the widespread importance of this metabolism, challenges remain in identifying denitrifying populations and predicting their metabolic end-products based on their genotype. Here, genome-resolved metagenomics was used to explore the denitrification genotype of <i>Bacillota</i> enriched in nitrate-amended high temperature incubations with confirmed N<sub>2</sub>O and N<sub>2</sub> production. A set of 12 hidden Markov models (HMMs) was created to target the diversity of denitrification genes in members of the phylum <i>Bacillota</i>. Genomic potential for complete denitrification was found in five metagenome-assembled genomes from nitrate-amended enrichments, including two novel members of the <i>Brevibacillaceae</i> family. Genomes of complete denitrifiers encode N<sub>2</sub>O reductase gene clusters with clade II-type <i>nosZ</i> and often include multiple variants of the nitric oxide reductase gene<i>.</i> The HMM set applied to all genomes of <i>Bacillota</i> from the Genome Taxonomy Database identified 17 genera inferred to contain complete denitrifiers based on their gene content. Among complete denitrifiers it was common for three distinct nitric oxide reductases to be present (qNOR, bNOR, and sNOR) that may reflect the metabolic adaptability of <i>Bacillota</i> in environments with variable redox conditions.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae107"},"PeriodicalIF":5.1,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11388526/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302629","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}
ISME communicationsPub Date : 2024-08-29eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae109
Julie Thomy, Frederic Sanchez, Camille Prioux, Sheree Yau, Yangbing Xu, Julian Mak, Ruixian Sun, Gwenael Piganeau, Charmaine C M Yung
{"title":"Unveiling <i>Prasinovirus</i> diversity and host specificity through targeted enrichment in the South China Sea.","authors":"Julie Thomy, Frederic Sanchez, Camille Prioux, Sheree Yau, Yangbing Xu, Julian Mak, Ruixian Sun, Gwenael Piganeau, Charmaine C M Yung","doi":"10.1093/ismeco/ycae109","DOIUrl":"https://doi.org/10.1093/ismeco/ycae109","url":null,"abstract":"<p><p>Unicellular green picophytoplankton from the Mamiellales order are pervasive in marine ecosystems and susceptible to infections by prasinoviruses, large double-stranded DNA viruses within the <i>Nucleocytoviricota</i> phylum. We developed a double-stranded DNA virus enrichment and shotgun sequencing method, and successfully assembled 80 prasinovirus genomes from 43 samples in the South China Sea. Our research delivered the first direct estimation of 94% accuracy in correlating genome similarity to host range. Stirkingly, our analyses uncovered unexpected host-switching across diverse algal lineages, challenging the existing paradigms of host-virus co-speciation and revealing the dynamic nature of viral evolution. We also detected six instances of horizontal gene transfer between prasinoviruses and their hosts, including a novel alternative oxidase. Additionally, diversifying selection on a major capsid protein suggests an ongoing co-evolutionary arms race. These insights not only expand our understanding of prasinovirus genomic diversity but also highlight the intricate evolutionary mechanisms driving their ecological success and shaping broader virus-host interactions in marine environments.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae109"},"PeriodicalIF":5.1,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11408933/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302631","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}
ISME communicationsPub Date : 2024-08-27eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae108
Amelia R Nelson, Charles C Rhoades, Timothy S Fegel, Holly K Roth, Marcos V Caiafa, Sydney I Glassman, Thomas Borch, Michael J Wilkins
{"title":"Wildfire impact on soil microbiome life history traits and roles in ecosystem carbon cycling.","authors":"Amelia R Nelson, Charles C Rhoades, Timothy S Fegel, Holly K Roth, Marcos V Caiafa, Sydney I Glassman, Thomas Borch, Michael J Wilkins","doi":"10.1093/ismeco/ycae108","DOIUrl":"10.1093/ismeco/ycae108","url":null,"abstract":"<p><p>Wildfires, which are increasing in frequency and severity with climate change, reduce soil microbial biomass and alter microbial community composition and function. The soil microbiome plays a vital role in carbon (C) and nitrogen (N) cycling, but its complexity makes it challenging to predict post-wildfire soil microbial dynamics and resulting impacts on ecosystem biogeochemistry. The application of biogeochemically relevant conceptual trait-based frameworks to the soil microbiome can distill this complexity, enabling enhanced predictability of soil microbiome recovery following wildfire and subsequent impacts to biogeochemical cycles. Conceptual frameworks that have direct links to soil C and N cycling have been developed for the soil microbiome; the Y-A-S framework overviews soil microbiome life history strategies that have tradeoffs with one another and others have proposed frameworks specific to wildfire. Here, we aimed to delineate post-wildfire changes of bacterial traits in western US coniferous forests to inform how severe wildfire influences soil microbiome recovery and resultant biogeochemical cycling. We utilized a comprehensive metagenome-assembled genome catalog from post-wildfire soils representing 1 to 11 years following low- and high-severity burning to identify traits that enable the persistence of microbial taxa in burned soils and influence ecosystem C and N cycling. We found that high-severity wildfire initially selects for fast growers and, up to a decade post-fire, taxa that invest in genes for acquiring diverse resources from the external environment, which in combination could increase soil C losses. This work begins to disentangle how climate change-induced shifts in wildfire behavior might alter microbially mediated soil biogeochemical cycling.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae108"},"PeriodicalIF":5.1,"publicationDate":"2024-08-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11831523/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143442790","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}
{"title":"A nanoluciferase-encoded bacteriophage illuminates viral infection dynamics of <i>Pseudomonas aeruginosa</i> cells.","authors":"Sophia Zborowsky, Quentin Balacheff, Ioanna Theodorou, Rokhaya Kane, Raphaëlle Delattre, Joshua S Weitz, Régis Tournebize, Laurent Debarbieux","doi":"10.1093/ismeco/ycae105","DOIUrl":"https://doi.org/10.1093/ismeco/ycae105","url":null,"abstract":"<p><p>Bacteriophages (phages) are increasingly considered for both treatment and early detection of bacterial pathogens given their specificity and rapid infection kinetics. Here, we exploit an engineered phage expressing nanoluciferase to detect signals associated with <i>Pseudomonas aeruginosa</i> lysis spanning single cells to populations. Using several <i>P. aeruginosa</i> strains we found that the latent period, burst size, fraction of infected cells, and efficiency of plating inferred from fluorescent light intensity signals were consistent with inferences from conventional population assays. Notably, imaging-based traits were obtained in minutes to hours in contrast to the use of overnight plaques, which opens the possibility to study infection dynamics in spatial and/or temporal contexts where plaque development is infeasible. These findings support the use of engineered phages to study infection kinetics of virus-cell interactions in complex environments and potentially accelerate the determination of viral host range in therapeutically relevant contexts.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae105"},"PeriodicalIF":5.1,"publicationDate":"2024-08-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11409504/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302628","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}
ISME communicationsPub Date : 2024-08-20eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae106
Lijuan Li, Songcan Chen, Ximei Xue, Jieyin Chen, Jian Tian, Lijuan Huo, Tuo Zhang, Xibai Zeng, Shiming Su
{"title":"Purifying selection drives distinctive arsenic metabolism pathways in prokaryotic and eukaryotic microbes.","authors":"Lijuan Li, Songcan Chen, Ximei Xue, Jieyin Chen, Jian Tian, Lijuan Huo, Tuo Zhang, Xibai Zeng, Shiming Su","doi":"10.1093/ismeco/ycae106","DOIUrl":"10.1093/ismeco/ycae106","url":null,"abstract":"<p><p>Microbes play a crucial role in the arsenic biogeochemical cycle through specific metabolic pathways to adapt to arsenic toxicity. However, the different arsenic-detoxification strategies between prokaryotic and eukaryotic microbes are poorly understood. This hampers our comprehension of how microbe-arsenic interactions drive the arsenic cycle and the development of microbial methods for remediation. In this study, we utilized conserved protein domains from 16 arsenic biotransformation genes (ABGs) to search for homologous proteins in 670 microbial genomes. Prokaryotes exhibited a wider species distribution of arsenic reduction- and arsenic efflux-related genes than fungi, whereas arsenic oxidation-related genes were more prevalent in fungi than in prokaryotes. This was supported by significantly higher <i>acr3</i> (arsenite efflux permease) expression in bacteria (upregulated 3.72-fold) than in fungi (upregulated 1.54-fold) and higher <i>aoxA</i> (arsenite oxidase) expression in fungi (upregulated 5.11-fold) than in bacteria (upregulated 2.05-fold) under arsenite stress. The average values of nonsynonymous substitutions per nonsynonymous site to synonymous substitutions per synonymous site (dN/dS) of homologous ABGs were higher in archaea (0.098) and bacteria (0.124) than in fungi (0.051). Significant negative correlations between the dN/dS of ABGs and species distribution breadth and gene expression levels in archaea, bacteria, and fungi indicated that microbes establish the distinct strength of purifying selection for homologous ABGs. These differences contribute to the distinct arsenic metabolism pathways in prokaryotic and eukaryotic microbes. These observations facilitate a significant shift from studying individual or several ABGs to characterizing the comprehensive microbial strategies of arsenic detoxification.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae106"},"PeriodicalIF":5.1,"publicationDate":"2024-08-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11370035/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142127520","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}
ISME communicationsPub Date : 2024-08-08eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae103
Maryam Mahmoudi, Juliana Almario, Katrina Lutap, Kay Nieselt, Eric Kemen
{"title":"Microbial communities living inside plant leaves or on the leaf surface are differently shaped by environmental cues.","authors":"Maryam Mahmoudi, Juliana Almario, Katrina Lutap, Kay Nieselt, Eric Kemen","doi":"10.1093/ismeco/ycae103","DOIUrl":"10.1093/ismeco/ycae103","url":null,"abstract":"<p><p>Leaf-associated microbial communities can promote plant health and resistance to biotic and abiotic stresses. However, the importance of environmental cues in the assembly of the leaf endo- and epi-microbiota remains elusive. Here, we aimed to investigate the impact of seasonal environmental variations, on the establishment of the leaf microbiome, focusing on long-term changes (five years) in bacterial, fungal, and nonfungal eukaryotic communities colonizing the surface and endosphere of six wild <i>Arabidopsis thaliana</i> populations. While leaf-microbial communities were found to be highly stochastic, the leaf niche had a predominant importance with endophytic microbial communities consistently exhibiting a lower diversity and variability. Among environmental factors, radiation- and humidity-related factors are the most important drivers of diversity patterns in the leaf, with stronger effects on epiphytic communities. Using linear models, we identified 30 important genera whose relative abundance in leaf compartments could be modeled from environmental variables, suggesting specific niche preferences for these taxa. With the hypothesis that environmental factors could impact interactions within microbial communities, we analyzed the seasonal patterns of microbial interaction networks across leaf compartments. We showed that epiphytic networks are more complex than endophytic and that the complexity and connectivity of these networks are partially correlated with the mentioned environmental cues. Our results indicate that humidity and solar radiation function as major environmental cues shaping the phyllosphere microbiome at both micro (leaf compartment) and macro (site) scales. These findings could have practical implications for predicting and developing field-adapted microbes in the face of global change.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae103"},"PeriodicalIF":5.1,"publicationDate":"2024-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11333920/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142010038","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}
ISME communicationsPub Date : 2024-08-07eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae104
Louis Berrios, Andressa M Venturini, Tillson Bertie Ansell, Esther Tok, William Johnson, Claire E Willing, Kabir G Peay
{"title":"Co-inoculations of bacteria and mycorrhizal fungi often drive additive plant growth responses.","authors":"Louis Berrios, Andressa M Venturini, Tillson Bertie Ansell, Esther Tok, William Johnson, Claire E Willing, Kabir G Peay","doi":"10.1093/ismeco/ycae104","DOIUrl":"10.1093/ismeco/ycae104","url":null,"abstract":"<p><p>Controlled greenhouse studies have shown the numerous ways that soil microbes can impact plant growth and development. However, natural soil communities are highly complex, and plants interact with many bacterial and fungal taxa simultaneously. Due to logistical challenges associated with manipulating more complex microbiome communities, how microbial communities impact emergent patterns of plant growth therefore remains poorly understood. For instance, do the interactions between bacteria and fungi generally yield additive (i.e. sum of their parts) or nonadditive, higher order plant growth responses? Without this information, our ability to accurately predict plant responses to microbial inoculants is weakened. To address these issues, we conducted a meta-analysis to determine the type (additive or higher-order, nonadditive interactions), frequency, direction (positive or negative), and strength that bacteria and mycorrhizal fungi (arbuscular and ectomycorrhizal) have on six phenotypic plant growth responses. Our results demonstrate that co-inoculations of bacteria and mycorrhizal fungi tend to have positive additive effects on many commonly reported plant responses. However, ectomycorrhizal plant shoot height responds positively and nonadditively to co-inoculations of bacteria and ectomycorrhizal fungi, and the strength of additive effects also differs between mycorrhizae type. These findings suggest that inferences from greenhouse studies likely scale to more complex field settings and that inoculating plants with diverse, beneficial microbes is a sound strategy to support plant growth.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae104"},"PeriodicalIF":5.1,"publicationDate":"2024-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11346365/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142074680","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}
ISME communicationsPub Date : 2024-08-02eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae101
Tara C J Spencer-Drakes, Angel Sarabia, Gary Heussler, Emily C Pierce, Manon Morin, Steven Villareal, Rachel J Dutton
{"title":"Phage resistance mutations affecting the bacterial cell surface increase susceptibility to fungi in a model cheese community.","authors":"Tara C J Spencer-Drakes, Angel Sarabia, Gary Heussler, Emily C Pierce, Manon Morin, Steven Villareal, Rachel J Dutton","doi":"10.1093/ismeco/ycae101","DOIUrl":"https://doi.org/10.1093/ismeco/ycae101","url":null,"abstract":"<p><p>Diverse populations of bacteriophages infect and coevolve with their bacterial hosts. Although host recognition and infection occur within microbiomes, the molecular mechanisms underlying host-phage interactions within a community context remain poorly studied. The biofilms (rinds) of aged cheeses contain taxonomically diverse microbial communities that follow reproducible growth patterns and can be manipulated under laboratory conditions. In this study, we use cheese as a model for studying phage-microbe interactions by identifying and characterizing a tractable host-phage pair co-occurring within a model Brie-like community. We isolated a novel bacteriophage, TS33, that kills <i>Hafnia</i> sp. JB232, a member of the model community. TS33 is easily propagated in the lab and naturally co-occurs in the cheese community, rendering it a prime candidate for the study of host-phage interactions. We performed growth assays of the <i>Hafnia</i>, TS33, and the fungal community members, <i>Geotrichum candidum</i> and <i>Penicillium camemberti</i>. Employing Random Barcode Transposon Sequencing experiments, we identified candidate host factors that contribute to TS33 infectivity, many of which are homologs of bacterial O-antigen genes. <i>Hafnia</i> mutants in these genes exhibit decreased susceptibility to phage infection, but experience negative fitness effects in the presence of the fungi. Therefore, mutations in O-antigen biosynthesis homologs may have antagonistic pleiotropic effects in <i>Hafnia</i> that have major consequences for its interactions with the rest of the community. Ongoing and future studies aim to unearth the molecular mechanisms by which the O-antigen of <i>Hafnia</i> mediates its interactions with its viral and fungal partners.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae101"},"PeriodicalIF":5.1,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11409937/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302630","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}
ISME communicationsPub Date : 2024-08-01eCollection Date: 2024-01-01DOI: 10.1093/ismeco/ycae102
Cesar T Facimoto, Kendall D Clements, W Lindsey White, Kim M Handley
{"title":"<i>Bacteroidia</i> and <i>Clostridia</i> are equipped to degrade a cascade of polysaccharides along the hindgut of the herbivorous fish <i>Kyphosus sydneyanus</i>.","authors":"Cesar T Facimoto, Kendall D Clements, W Lindsey White, Kim M Handley","doi":"10.1093/ismeco/ycae102","DOIUrl":"10.1093/ismeco/ycae102","url":null,"abstract":"<p><p>The gut microbiota of the marine herbivorous fish <i>Kyphosus sydneyanus</i> are thought to play an important role in host nutrition by supplying short-chain fatty acids (SCFAs) through fermentation of dietary red and brown macroalgae. Here, using 645 metagenome-assembled genomes (MAGs) from wild fish, we determined the capacity of different bacterial taxa to degrade seaweed carbohydrates along the gut. Most bacteria (99%) were unclassified at the species level. Gut communities and CAZyme-related transcriptional activity were dominated by <i>Bacteroidia</i> and <i>Clostridia</i>. Both classes possess genes CAZymes acting on internal polysaccharide bonds, suggesting their role initiating glycan depolymerization, followed by rarer <i>Gammaproteobacteria</i> and <i>Verrucomicrobiae</i>. Results indicate that <i>Bacteroidia</i> utilize substrates in both brown and red algae, whereas other taxa, namely, <i>Clostridia</i>, <i>Bacilli</i>, and <i>Verrucomicrobiae</i>, utilize mainly brown algae. <i>Bacteroidia</i> had the highest CAZyme gene densities overall, and <i>Alistipes</i> were especially enriched in CAZyme gene clusters (<i>n</i> = 73 versus just 62 distributed across all other taxa), pointing to an enhanced capacity for macroalgal polysaccharide utilization (e.g., alginate, laminarin, and sulfated polysaccharides). Pairwise correlations of MAG relative abundances and encoded CAZyme compositions provide evidence of potential inter-species collaborations. Co-abundant MAGs exhibited complementary degradative capacities for specific substrates, and flexibility in their capacity to source carbon (e.g., glucose- or galactose-rich glycans), possibly facilitating coexistence via niche partitioning. Results indicate the potential for collaborative microbial carbohydrate metabolism in the <i>K. sydneyanus</i> gut, that a greater variety of taxa contribute to the breakdown of brown versus red dietary algae, and that <i>Bacteroidia</i> encompass specialized macroalgae degraders.</p>","PeriodicalId":73516,"journal":{"name":"ISME communications","volume":"4 1","pages":"ycae102"},"PeriodicalIF":5.1,"publicationDate":"2024-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11333855/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142010037","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}