Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics

Yu, Xiaoqian Annie; McLean, Craig; Hehemann, Jan-Hendrik; Angeles-Albores, David; Wu, Fuqing; Muszyński, Artur; Corzett, Christopher H.; Azadi, Parastoo; Kujawinski, Elizabeth B.; Alm, Eric J.; Polz, Martin F.

doi:10.1093/ismejo/wrad013

Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics

Journal Article · Wed Jan 10 00:00:00 EST 2024 · The ISME Journal

DOI:https://doi.org/10.1093/ismejo/wrad013· OSTI ID:2282178

Yu, Xiaoqian Annie ^[1]; McLean, Craig ^[2]; Hehemann, Jan-Hendrik ^[3]; Angeles-Albores, David ^[3]; Wu, Fuqing ^[3]; Muszyński, Artur ^[4]; Corzett, Christopher H. ^[3]; Azadi, Parastoo ^[4]; Kujawinski, Elizabeth B. ^[2]; Alm, Eric J. ^[5]; Polz, Martin F. ^[6]

Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); University of Vienna (Austria)
Woods Hole Oceanographic Institution, MA (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)
University of Georgia, Athens, GA (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); Harvard University, Cambridge, MA (United States)
University of Vienna (Austria); Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)

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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Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States); Univ. of Georgia, Athens, GA (United States); University of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0008743; SC0015662

OSTI ID:: 2282178

Alternate ID(s):: OSTI ID: 2471954
OSTI ID: 2530537

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 1 Vol. 18; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Low-level resource partitioning supports coexistence among functionally redundant bacteria during successional dynamics

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