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Metabolic flexibility allows bacterial habitat generalists to become dominant in a frequently disturbed ecosystem

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posted on 08.12.2021, 02:54 by YJ Chen, PM Leung, Jennifer WoodJennifer Wood, SK Bay, P Hugenholtz, AJ Kessler, G Shelley, DW Waite, Ashley FranksAshley Franks, PLM Cook, C Greening
Ecological theory suggests that habitat disturbance differentially influences distributions of habitat generalist and specialist species. While well-established for macroorganisms, this theory has rarely been explored for microorganisms. Here we tested these principles in permeable (sandy) sediments, ecosystems with much spatiotemporal variation in resource availability and physicochemical conditions. Microbial community composition and function were profiled in intertidal and subtidal sediments using 16S rRNA gene amplicon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Community composition and metabolic traits modestly varied with sediment depth and sampling date. Several taxa were highly abundant and prevalent in all samples, including within the orders Woeseiales and Flavobacteriales, and classified as habitat generalists; genome reconstructions indicate these taxa are highly metabolically flexible facultative anaerobes and adapt to resource variability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers and candidate lineage MBNT15 were less abundant overall and only thrived in more stable deeper sediments. We substantiated these findings by measuring three metabolic processes in these sediments; whereas the habitat generalist-associated processes of sulfide oxidation and fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. A manipulative experiment also confirmed habitat generalists outcompete specialist taxa during simulated habitat disturbance. Together, these findings show metabolically flexible habitat generalists become dominant in highly dynamic environments, whereas metabolically constrained specialists are restricted to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.

Funding

This study was supported by an ARC Discovery Project (DP180101762; awarded to PLMC and CG), an ARC DECRA Fellowship (DE170100310; salary for CG), an ARC Laureate Fellowship (FL150100038; awarded to PH), an NHMRC EL2 Fellowship (APP1178715; salary for CG), Monash International Tuition Scholarships (awarded to YJC, PML and SKB), Australian Government Research Training Stipends (awarded to PML and SKB), and a PhD scholarship from the Taiwan Ministry of Education (awarded to YJC).

History

Publication Date

01/10/2021

Journal

ISME Journal

Volume

15

Issue

10

Pagination

2986-3004

Publisher

Springer Nature

ISSN

1751-7362

Rights Statement

© The Author(s) 2021 This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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