Low-abundance populations distinguish microbiome performance in plant cell wall deconstruction

Lauren M Tom; Martina Aulitto; Yu-Wei Wu; Kai Deng; Yu Gao; Naijia Xiao; Beatrice Garcia Rodriguez; Clifford Louime; Trent R Northen; Aymerick Eudes; Jenny C Mortimer; Paul D Adams; Henrik V Scheller; Blake A Simmons; Javier A Ceja-Navarro; Steven W Singer

doi:10.1186/s40168-022-01377-x

Low-abundance populations distinguish microbiome performance in plant cell wall deconstruction

Microbiome. 2022 Oct 25;10(1):183. doi: 10.1186/s40168-022-01377-x.

Authors

Lauren M Tom^#^{1

2}, Martina Aulitto^#^{1

2}, Yu-Wei Wu³, Kai Deng^{1

2}, Yu Gao^{1

4}, Naijia Xiao⁵, Beatrice Garcia Rodriguez⁶, Clifford Louime⁶, Trent R Northen^{1

4}, Aymerick Eudes^{1

4}, Jenny C Mortimer^{1

4

7}, Paul D Adams^{1

8

9}, Henrik V Scheller^{1

4

10}, Blake A Simmons^{1

2}, Javier A Ceja-Navarro^{11

12

13

14}, Steven W Singer^{15

16}

Affiliations

¹ Joint BioEnergy Institute, Emeryville, CA, USA.
² Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
³ Graduate Institute of Biomedical Informatics, College of Medical Science and Technology, Taipei Medical University, Taipei, 110, Taiwan.
⁴ Environmental Systems and Genome Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁵ Institute of Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, USA.
⁶ College of Natural Sciences, University of Puerto Rico, Rio Piedras, Puerto Rico.
⁷ School of Agriculture, Food and Wine, & Waite Research Institute, University of Adelaide, Glen Osmond, SA, Australia.
⁸ Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁹ Department of Bioengineering, University of California Berkeley, Berkeley, CA, USA.
¹⁰ Department of Plant and Microbial Biology, University of California-Berkeley, Berkeley, CA, USA.
¹¹ Joint BioEnergy Institute, Emeryville, CA, USA. JCNavarro@lbl.gov.
¹² Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. JCNavarro@lbl.gov.
¹³ Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA. JCNavarro@lbl.gov.
¹⁴ Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, USA. JCNavarro@lbl.gov.
¹⁵ Joint BioEnergy Institute, Emeryville, CA, USA. SWSinger@lbl.gov.
¹⁶ Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA. SWSinger@lbl.gov.

^# Contributed equally.

Abstract

Background: Plant cell walls are interwoven structures recalcitrant to degradation. Native and adapted microbiomes can be particularly effective at plant cell wall deconstruction. Although most understanding of biological cell wall deconstruction has been obtained from isolates, cultivated microbiomes that break down cell walls have emerged as new sources for biotechnologically relevant microbes and enzymes. These microbiomes provide a unique resource to identify key interacting functional microbial groups and to guide the design of specialized synthetic microbial communities.

Results: To establish a system assessing comparative microbiome performance, parallel microbiomes were cultivated on sorghum (Sorghum bicolor L. Moench) from compost inocula. Biomass loss and biochemical assays indicated that these microbiomes diverged in their ability to deconstruct biomass. Network reconstructions from gene expression dynamics identified key groups and potential interactions within the adapted sorghum-degrading communities, including Actinotalea, Filomicrobium, and Gemmatimonadetes populations. Functional analysis demonstrated that the microbiomes proceeded through successive stages that are linked to enzymes that deconstruct plant cell wall polymers. The combination of network and functional analysis highlighted the importance of cellulose-degrading Actinobacteria in differentiating the performance of these microbiomes.

Conclusions: The two-tier cultivation of compost-derived microbiomes on sorghum led to the establishment of microbiomes for which community structure and performance could be assessed. The work reinforces the observation that subtle differences in community composition and the genomic content of strains may lead to significant differences in community performance. Video Abstract.

Keywords: Biomass deconstruction; Lignocellulose degradation; Microbiome; Transcriptomic network.

Publication types

Video-Audio Media
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Bacteria / genetics
Biomass
Cell Wall
Cellulose / chemistry
Microbiota*

Substances

Cellulose