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Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance
Although biotic interactions among members of microbial communities have been conceived to be crucial for community assembly, it remains unclear how changes in environmental conditions affect microbial interaction and consequently system performance. Here, we adopted a random matrix theory-based net...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946792/ https://www.ncbi.nlm.nih.gov/pubmed/31911462 http://dx.doi.org/10.1128/mSystems.00357-19 |
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author | Wu, Linwei Shan, Xiaoyu Chen, Si Zhang, Qiuting Qi, Qi Qin, Ziyan Yin, Huaqun Zhou, Jizhong He, Qiang Yang, Yunfeng |
author_facet | Wu, Linwei Shan, Xiaoyu Chen, Si Zhang, Qiuting Qi, Qi Qin, Ziyan Yin, Huaqun Zhou, Jizhong He, Qiang Yang, Yunfeng |
author_sort | Wu, Linwei |
collection | PubMed |
description | Although biotic interactions among members of microbial communities have been conceived to be crucial for community assembly, it remains unclear how changes in environmental conditions affect microbial interaction and consequently system performance. Here, we adopted a random matrix theory-based network analysis to explore microbial interactions in triplicate anaerobic digestion (AD) systems, which is widely applied for organic pollutant treatments. The digesters were operated with incremental organic loading rates (OLRs) from 1.0 g volatile solids (VS)/liter/day to 1.3 g VS/liter/day and then to 1.5 g VS/liter/day, which increased VS removal and methane production proportionally. Higher resource availability led to networks with higher connectivity and shorter harmonic geodesic distance, suggestive of more intense microbial interactions and quicker responses to environmental changes. Strikingly, a number of topological properties of microbial network showed significant (P < 0.05) correlation with AD performance (i.e., methane production, biogas production, and VS removal). When controlling for environmental parameters (e.g., total ammonia, pH, and the VS load), node connectivity, especially that of the methanogenic archaeal network, still correlated with AD performance. Last, we identified the Methanothermus, Methanobacterium, Chlorobium, and Haloarcula taxa and an unclassified Thaumarchaeota taxon as keystone nodes of the network. IMPORTANCE AD is a biological process widely used for effective waste treatment throughout the world. Biotic interactions among microbes are critical to the assembly and functioning of the microbial community, but the response of microbial interactions to environmental changes and their influence on AD performance are still poorly understood. Using well-replicated time series data of 16S rRNA gene amplicons and functional gene arrays, we constructed random matrix theory-based association networks to characterize potential microbial interactions with incremental OLRs. We demonstrated striking linkage between network topological features of methanogenic archaea and AD functioning independent of environmental parameters. As the intricate balance of multiple microbial functional groups is responsible for methane production, our results suggest that microbial interaction may be an important, previously unrecognized mechanism in determining AD performance. |
format | Online Article Text |
id | pubmed-6946792 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-69467922020-01-16 Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance Wu, Linwei Shan, Xiaoyu Chen, Si Zhang, Qiuting Qi, Qi Qin, Ziyan Yin, Huaqun Zhou, Jizhong He, Qiang Yang, Yunfeng mSystems Research Article Although biotic interactions among members of microbial communities have been conceived to be crucial for community assembly, it remains unclear how changes in environmental conditions affect microbial interaction and consequently system performance. Here, we adopted a random matrix theory-based network analysis to explore microbial interactions in triplicate anaerobic digestion (AD) systems, which is widely applied for organic pollutant treatments. The digesters were operated with incremental organic loading rates (OLRs) from 1.0 g volatile solids (VS)/liter/day to 1.3 g VS/liter/day and then to 1.5 g VS/liter/day, which increased VS removal and methane production proportionally. Higher resource availability led to networks with higher connectivity and shorter harmonic geodesic distance, suggestive of more intense microbial interactions and quicker responses to environmental changes. Strikingly, a number of topological properties of microbial network showed significant (P < 0.05) correlation with AD performance (i.e., methane production, biogas production, and VS removal). When controlling for environmental parameters (e.g., total ammonia, pH, and the VS load), node connectivity, especially that of the methanogenic archaeal network, still correlated with AD performance. Last, we identified the Methanothermus, Methanobacterium, Chlorobium, and Haloarcula taxa and an unclassified Thaumarchaeota taxon as keystone nodes of the network. IMPORTANCE AD is a biological process widely used for effective waste treatment throughout the world. Biotic interactions among microbes are critical to the assembly and functioning of the microbial community, but the response of microbial interactions to environmental changes and their influence on AD performance are still poorly understood. Using well-replicated time series data of 16S rRNA gene amplicons and functional gene arrays, we constructed random matrix theory-based association networks to characterize potential microbial interactions with incremental OLRs. We demonstrated striking linkage between network topological features of methanogenic archaea and AD functioning independent of environmental parameters. As the intricate balance of multiple microbial functional groups is responsible for methane production, our results suggest that microbial interaction may be an important, previously unrecognized mechanism in determining AD performance. American Society for Microbiology 2020-01-07 /pmc/articles/PMC6946792/ /pubmed/31911462 http://dx.doi.org/10.1128/mSystems.00357-19 Text en Copyright © 2020 Wu 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 Wu, Linwei Shan, Xiaoyu Chen, Si Zhang, Qiuting Qi, Qi Qin, Ziyan Yin, Huaqun Zhou, Jizhong He, Qiang Yang, Yunfeng Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title | Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title_full | Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title_fullStr | Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title_full_unstemmed | Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title_short | Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance |
title_sort | progressive microbial community networks with incremental organic loading rates underlie higher anaerobic digestion performance |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946792/ https://www.ncbi.nlm.nih.gov/pubmed/31911462 http://dx.doi.org/10.1128/mSystems.00357-19 |
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