Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics
Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics
Date
2024-01-10
Authors
Yu, Xiaoqian Annie
McLean, Craig
Hehemann, Jan-Hendrik
Angeles-Albores, David
Wu, Fuqing
Muszynski, Artur
Corzett, Christopher H.
Azadi, Parastoo
Kujawinski, Elizabeth B.
Alm, Eric J.
Polz, Martin F.
McLean, Craig
Hehemann, Jan-Hendrik
Angeles-Albores, David
Wu, Fuqing
Muszynski, Artur
Corzett, Christopher H.
Azadi, Parastoo
Kujawinski, Elizabeth B.
Alm, Eric J.
Polz, Martin F.
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DOI
10.1093/ismejo/wrad013
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Keywords
Functional redundancy
Resource partitioning
Coexistence
Community assembly
Resource partitioning
Coexistence
Community assembly
Abstract
Members of microbial communities can substantially overlap in substrate use. However, what enables functionally redundant microorganisms to coassemble or even stably coexist remains poorly understood. Here, we show that during unstable successional dynamics on complex, natural organic matter, functionally redundant bacteria can coexist by partitioning low-concentration substrates even though they compete for one simple, dominant substrate. We allowed ocean microbial communities to self-assemble on leachates of the brown seaweed Fucus vesiculosus and then analyzed the competition among 10 taxonomically diverse isolates representing two distinct stages of the succession. All, but two isolates, exhibited an average of 90% ± 6% pairwise overlap in resource use, and functional redundancy of isolates from the same assembly stage was higher than that from between assembly stages, leading us to construct a simpler four-isolate community with two isolates from each of the early and late stages. We found that, although the short-term dynamics of the four-isolate communities in F. vesiculosus leachate was dependent on initial isolate ratios, in the long term, the four isolates stably coexist in F. vesiculosus leachate, albeit with some strains at low abundance. We therefore explored the potential for nonredundant substrate use by genomic content analysis and RNA expression patterns. This analysis revealed that the four isolates mainly differed in peripheral metabolic pathways, such as the ability to degrade pyrimidine, leucine, and tyrosine, as well as aromatic substrates. These results highlight the importance of fine-scale differences in metabolic strategies for supporting the frequently observed coexistence of large numbers of rare organisms in natural microbiomes.
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© The Author(s), 2024. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Yu, X., McLean, C., Hehemann, J.-H., Angeles-Albores, D., Wu, F., Muszyński, A., Corzett, C., Azadi, P., Kujawinski, E., Alm, E., & Polz, M. (2024). Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics. The ISME Journal: Multidisciplinary Journal of Microbial Ecology, wrad013, https://doi.org/10.1093/ismejo/wrad013.
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Yu, X., McLean, C., Hehemann, J.-H., Angeles-Albores, D., Wu, F., Muszyński, A., Corzett, C., Azadi, P., Kujawinski, E., Alm, E., & Polz, M. (2024). Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics. The ISME Journal: Multidisciplinary Journal of Microbial Ecology, wrad013.