Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance

ABSTRACT 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-...

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Autores principales:	Linwei Wu, Xiaoyu Shan, Si Chen, Qiuting Zhang, Qi Qi, Ziyan Qin, Huaqun Yin, Jizhong Zhou, Qiang He, Yunfeng Yang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	anaerobic digestion microbial interaction system performance Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2e6ea9a27be944cf855c2d5a99412626
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spelling	oai:doaj.org-article:2e6ea9a27be944cf855c2d5a994126262021-12-02T19:46:20ZProgressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance10.1128/mSystems.00357-192379-5077https://doaj.org/article/2e6ea9a27be944cf855c2d5a994126262020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00357-19https://doaj.org/toc/2379-5077ABSTRACT 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.Linwei WuXiaoyu ShanSi ChenQiuting ZhangQi QiZiyan QinHuaqun YinJizhong ZhouQiang HeYunfeng YangAmerican Society for Microbiologyarticleanaerobic digestionmicrobial interactionsystem performanceMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	anaerobic digestion microbial interaction system performance Microbiology QR1-502
spellingShingle	anaerobic digestion microbial interaction system performance Microbiology QR1-502 Linwei Wu Xiaoyu Shan Si Chen Qiuting Zhang Qi Qi Ziyan Qin Huaqun Yin Jizhong Zhou Qiang He Yunfeng Yang Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance
description	ABSTRACT 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	article
author	Linwei Wu Xiaoyu Shan Si Chen Qiuting Zhang Qi Qi Ziyan Qin Huaqun Yin Jizhong Zhou Qiang He Yunfeng Yang
author_facet	Linwei Wu Xiaoyu Shan Si Chen Qiuting Zhang Qi Qi Ziyan Qin Huaqun Yin Jizhong Zhou Qiang He Yunfeng Yang
author_sort	Linwei Wu
title	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_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_sort	progressive microbial community networks with incremental organic loading rates underlie higher anaerobic digestion performance
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/2e6ea9a27be944cf855c2d5a99412626
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_version_	1718376016266657792

Progressive Microbial Community Networks with Incremental Organic Loading Rates Underlie Higher Anaerobic Digestion Performance

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