Cargando…
Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods
The complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as th...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040578/ https://www.ncbi.nlm.nih.gov/pubmed/35258341 http://dx.doi.org/10.1128/msystems.01519-21 |
_version_ | 1784694365094936576 |
---|---|
author | Lewin, Gina R. Davis, Nicole M. McDonald, Bradon R. Book, Adam J. Chevrette, Marc G. Suh, Steven Boll, Ardina Currie, Cameron R. |
author_facet | Lewin, Gina R. Davis, Nicole M. McDonald, Bradon R. Book, Adam J. Chevrette, Marc G. Suh, Steven Boll, Ardina Currie, Cameron R. |
author_sort | Lewin, Gina R. |
collection | PubMed |
description | The complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as the sole source of carbon, we examine how changes in bacterial diversity and interactions impact plant biomass decomposition. Over up to 60 serial transfers (∼8 months) using Whatman cellulose filter paper, cellulolytic ability increased and then stabilized in four enrichment lines and was variable in two lines. Bacterial community characterization using 16S rRNA gene amplicon sequencing showed community succession differed between the highly cellulolytic enrichment lines and those that had slower and more variable cellulose degradation rates. Metagenomic and metatranscriptomic analyses revealed that Cellvibrio and/or Cellulomonas dominated each enrichment line and produced the majority of cellulase enzymes, while diverse taxa were retained within these communities over the duration of transfers. Interestingly, the less cellulolytic communities had a higher diversity of organisms competing for the cellulose breakdown product cellobiose, suggesting that cheating slowed cellulose degradation. In addition, we found competitive exclusion as an important factor shaping all of the communities, with a negative correlation of Cellvibrio and Cellulomonas abundance within individual enrichment lines and the expression of genes associated with the production of secondary metabolites, toxins, and other antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities. IMPORTANCE Microbial communities are a key driver of the carbon cycle through the breakdown of complex polysaccharides in diverse environments including soil, marine systems, and the mammalian gut. However, due to the complexity of these communities, the species-species interactions that impact community structure and ultimately shape the rate of decomposition are difficult to define. Here, we performed serial enrichment on cellulose using communities inoculated from leaf-cutter ant refuse dumps, a cellulose-rich environment. By concurrently tracking cellulolytic ability and community composition and through metagenomic and metatranscriptomic sequencing, we analyzed the ecological dynamics of the enrichment lines. Our data suggest that antagonism is prevalent in these communities and that competition for soluble sugars may slow degradation and lead to community instability. Together, these results help reveal the relationships between competition and polysaccharide decomposition, with implications in diverse areas ranging from microbial community ecology to cellulosic biofuels production. |
format | Online Article Text |
id | pubmed-9040578 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-90405782022-04-27 Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods Lewin, Gina R. Davis, Nicole M. McDonald, Bradon R. Book, Adam J. Chevrette, Marc G. Suh, Steven Boll, Ardina Currie, Cameron R. mSystems Research Article The complexity of microbial communities hinders our understanding of how microbial diversity and microbe-microbe interactions impact community functions. Here, using six independent communities originating from the refuse dumps of leaf-cutter ants and enriched using the plant polymer cellulose as the sole source of carbon, we examine how changes in bacterial diversity and interactions impact plant biomass decomposition. Over up to 60 serial transfers (∼8 months) using Whatman cellulose filter paper, cellulolytic ability increased and then stabilized in four enrichment lines and was variable in two lines. Bacterial community characterization using 16S rRNA gene amplicon sequencing showed community succession differed between the highly cellulolytic enrichment lines and those that had slower and more variable cellulose degradation rates. Metagenomic and metatranscriptomic analyses revealed that Cellvibrio and/or Cellulomonas dominated each enrichment line and produced the majority of cellulase enzymes, while diverse taxa were retained within these communities over the duration of transfers. Interestingly, the less cellulolytic communities had a higher diversity of organisms competing for the cellulose breakdown product cellobiose, suggesting that cheating slowed cellulose degradation. In addition, we found competitive exclusion as an important factor shaping all of the communities, with a negative correlation of Cellvibrio and Cellulomonas abundance within individual enrichment lines and the expression of genes associated with the production of secondary metabolites, toxins, and other antagonistic compounds. Our results provide insights into how microbial diversity and competition affect the stability and function of cellulose-degrading communities. IMPORTANCE Microbial communities are a key driver of the carbon cycle through the breakdown of complex polysaccharides in diverse environments including soil, marine systems, and the mammalian gut. However, due to the complexity of these communities, the species-species interactions that impact community structure and ultimately shape the rate of decomposition are difficult to define. Here, we performed serial enrichment on cellulose using communities inoculated from leaf-cutter ant refuse dumps, a cellulose-rich environment. By concurrently tracking cellulolytic ability and community composition and through metagenomic and metatranscriptomic sequencing, we analyzed the ecological dynamics of the enrichment lines. Our data suggest that antagonism is prevalent in these communities and that competition for soluble sugars may slow degradation and lead to community instability. Together, these results help reveal the relationships between competition and polysaccharide decomposition, with implications in diverse areas ranging from microbial community ecology to cellulosic biofuels production. American Society for Microbiology 2022-03-08 /pmc/articles/PMC9040578/ /pubmed/35258341 http://dx.doi.org/10.1128/msystems.01519-21 Text en Copyright © 2022 Lewin et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Lewin, Gina R. Davis, Nicole M. McDonald, Bradon R. Book, Adam J. Chevrette, Marc G. Suh, Steven Boll, Ardina Currie, Cameron R. Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title | Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title_full | Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title_fullStr | Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title_full_unstemmed | Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title_short | Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods |
title_sort | long-term cellulose enrichment selects for highly cellulolytic consortia and competition for public goods |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9040578/ https://www.ncbi.nlm.nih.gov/pubmed/35258341 http://dx.doi.org/10.1128/msystems.01519-21 |
work_keys_str_mv | AT lewinginar longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT davisnicolem longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT mcdonaldbradonr longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT bookadamj longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT chevrettemarcg longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT suhsteven longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT bollardina longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods AT curriecameronr longtermcelluloseenrichmentselectsforhighlycellulolyticconsortiaandcompetitionforpublicgoods |