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Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy

INTRODUCTION: Understanding how microorganisms within a soil community interact to support collective respiration and growth remains challenging. Here, we used a model substrate, chitin, and a synthetic Model Soil Consortium (MSC-2) to investigate how individual members of a microbial community cont...

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Autores principales: McClure, Ryan, Garcia, Marci, Couvillion, Sneha, Farris, Yuliya, Hofmockel, Kirsten S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9902710/
https://www.ncbi.nlm.nih.gov/pubmed/36762098
http://dx.doi.org/10.3389/fmicb.2022.1046661
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author McClure, Ryan
Garcia, Marci
Couvillion, Sneha
Farris, Yuliya
Hofmockel, Kirsten S.
author_facet McClure, Ryan
Garcia, Marci
Couvillion, Sneha
Farris, Yuliya
Hofmockel, Kirsten S.
author_sort McClure, Ryan
collection PubMed
description INTRODUCTION: Understanding how microorganisms within a soil community interact to support collective respiration and growth remains challenging. Here, we used a model substrate, chitin, and a synthetic Model Soil Consortium (MSC-2) to investigate how individual members of a microbial community contribute to decomposition and community growth. While MSC-2 can grow using chitin as the sole carbon source, we do not yet know how the growth kinetics or final biomass yields of MSC-2 vary when certain chitin degraders, or other important members, are absent. METHODS: To characterize specific roles within this synthetic community, we carried out experiments leaving out members of MSC-2 and measuring biomass yields and CO(2) production. We chose two members to iteratively leave out (referred to by genus name): Streptomyces, as it is predicted via gene expression analysis to be a major chitin degrader in the community, and Rhodococcus as it is predicted via species co-abundance analysis to interact with several other members. RESULTS: Our results showed that when MSC-2 lacked Streptomyces, growth and respiration of the community was severely reduced. Removal of either Streptomyces or Rhodococcus led to major changes in abundance for several other species, pointing to a comprehensive shifting of the microbial community when important members are removed, as well as alterations in the metabolic profile, especially when Streptomyces was lacking. These results show that when keystone, chitin degrading members are removed, other members, even those with the potential to degrade chitin, do not fill the same metabolic niche to promote community growth. In addition, highly connected members may be removed with similar or even increased levels of growth and respiration. DISCUSSION: Our findings are critical to a better understanding of soil microbiology, specifically in how communities maintain activity when biotic or abiotic factors lead to changes in biodiversity in soil systems.
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spelling pubmed-99027102023-02-08 Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy McClure, Ryan Garcia, Marci Couvillion, Sneha Farris, Yuliya Hofmockel, Kirsten S. Front Microbiol Microbiology INTRODUCTION: Understanding how microorganisms within a soil community interact to support collective respiration and growth remains challenging. Here, we used a model substrate, chitin, and a synthetic Model Soil Consortium (MSC-2) to investigate how individual members of a microbial community contribute to decomposition and community growth. While MSC-2 can grow using chitin as the sole carbon source, we do not yet know how the growth kinetics or final biomass yields of MSC-2 vary when certain chitin degraders, or other important members, are absent. METHODS: To characterize specific roles within this synthetic community, we carried out experiments leaving out members of MSC-2 and measuring biomass yields and CO(2) production. We chose two members to iteratively leave out (referred to by genus name): Streptomyces, as it is predicted via gene expression analysis to be a major chitin degrader in the community, and Rhodococcus as it is predicted via species co-abundance analysis to interact with several other members. RESULTS: Our results showed that when MSC-2 lacked Streptomyces, growth and respiration of the community was severely reduced. Removal of either Streptomyces or Rhodococcus led to major changes in abundance for several other species, pointing to a comprehensive shifting of the microbial community when important members are removed, as well as alterations in the metabolic profile, especially when Streptomyces was lacking. These results show that when keystone, chitin degrading members are removed, other members, even those with the potential to degrade chitin, do not fill the same metabolic niche to promote community growth. In addition, highly connected members may be removed with similar or even increased levels of growth and respiration. DISCUSSION: Our findings are critical to a better understanding of soil microbiology, specifically in how communities maintain activity when biotic or abiotic factors lead to changes in biodiversity in soil systems. Frontiers Media S.A. 2023-01-24 /pmc/articles/PMC9902710/ /pubmed/36762098 http://dx.doi.org/10.3389/fmicb.2022.1046661 Text en Copyright © 2023 McClure, Garcia, Couvillion, Farris and Hofmockel. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
McClure, Ryan
Garcia, Marci
Couvillion, Sneha
Farris, Yuliya
Hofmockel, Kirsten S.
Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title_full Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title_fullStr Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title_full_unstemmed Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title_short Removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
title_sort removal of primary nutrient degraders reduces growth of soil microbial communities with genomic redundancy
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9902710/
https://www.ncbi.nlm.nih.gov/pubmed/36762098
http://dx.doi.org/10.3389/fmicb.2022.1046661
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