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.; Mackelprang, ed., Rachel

doi:10.1128/msystems.01519-21

Title: Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods

Journal Article · Tue Apr 26 00:00:00 EDT 2022 · mSystems

DOI:https://doi.org/10.1128/msystems.01519-21· OSTI ID:1853829

^[1]; Davis, Nicole M. ^[1]; McDonald, Bradon R. ^[2]; Book, Adam J. ^[1];

^[3]; Suh, Steven ^[1]; Boll, Ardina ^[1];

^[1]; Mackelprang, ed., Rachel

Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin—Madison, Madison, Wisconsin, USA, Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA, Wisconsin Institute for Discovery and Department of Plant Pathology, University of Wisconsin—Madison, Madison, Wisconsin, USA

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.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)

Grant/Contract Number:: FC02-07ER64494; DEB-1927155; DGE-1256259; T32 GM07215; T32 GM008505

OSTI ID:: 1853829

Alternate ID(s):: OSTI ID: 1904222

Journal Information:: mSystems, Journal Name: mSystems Vol. 7 Journal Issue: 2; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Atta colombica
cellulose degradation
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metatranscriptomics

Title: Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods

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