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...

Descripción completa

Detalles Bibliográficos
Autores principales: Lewin, Gina R., Davis, Nicole M., McDonald, Bradon R., Book, Adam J., Chevrette, Marc G., Suh, Steven, Boll, Ardina, Currie, Cameron R.
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