Metabolic interdependencies in thermophilic communities are revealed using co-occurrence and complementarity networks

Xi Peng, Shang Wang, Miaoxiao Wang, Kai Feng, Qing He, Xingsheng Yang, Weiguo Hou, Fangru Li, Yuxiang Zhao, Baolan Hu, Xiao Zou and Ye Deng ()
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Xi Peng: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)
Shang Wang: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)
Miaoxiao Wang: ETH Zürich
Kai Feng: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)
Qing He: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)
Xingsheng Yang: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)
Weiguo Hou: China University of Geosciences
Fangru Li: China University of Geosciences
Yuxiang Zhao: Zhejiang University
Baolan Hu: Zhejiang University
Xiao Zou: College of Life Sciences, Guizhou University
Ye Deng: Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences (CAS)

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract Microbial communities exhibit intricate interactions underpinned by metabolic dependencies. To elucidate these dependencies, we present a workflow utilizing random matrix theory on metagenome-assembled genomes to construct co-occurrence and metabolic complementarity networks. We apply this approach to a temperature gradient hot spring, unraveling the interplay between thermal stress and metabolic cooperation. Our analysis reveals an increase in the frequency of metabolic interactions with rising temperatures. Amino acids, coenzyme A derivatives, and carbohydrates emerge as key exchange metabolites, forming the foundation for syntrophic dependencies, in which commensalistic interactions take a greater proportion than mutualistic ones. These metabolic exchanges are most prevalent between phylogenetically distant species, especially archaea-bacteria collaborations, as a crucial adaptation to harsh environments. Furthermore, we identify a significant positive correlation between basal metabolite exchange and genome size disparity, potentially signifying a means for streamlined genomes to leverage cooperation with metabolically richer partners. This phenomenon is also confirmed by another composting system which has a similar wide range of temperature fluctuations. Our workflow provides a feasible way to decipher the metabolic complementarity mechanisms underlying microbial interactions, and our findings suggested environmental stress regulates the cooperative strategies of thermophiles, while these dependencies have been potentially hardwired into their genomes during co-evolutions.

Date: 2024
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DOI: 10.1038/s41467-024-52532-x

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