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

ABSTRACT: 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.

SUBMITTER: Chen YJ

PROVIDER: S-EPMC8443593 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:A core issue in microbial ecology is the need to elucidate the ecological processes and underlying mechanisms involved in microbial community assembly. However, the extent to which these mechanisms differ in importance based on traits of taxa with different niche breadth is poorly understood. Here, we used high-throughput sequencing to examine the relative importance of environmental selection and stochastic processes in shaping soil bacterial sub-communities with different niche breadth (including habitat generalists, specialists and other taxa) across elevational gradients on the subalpine slope of Mount Wutai, Northern China. Our findings suggested that the composition of soil bacterial communities differed significantly different among elevational gradients. According to the niche breadth index, 10.9% of OTUs were defined as habitat generalists (B-value >8.7) and 10.0% of OTUs were defined as habitat specialists (B-value <1.5). Generalists and specialists differed distinctly in diversity and biogeographic patterns across elevational gradients. Environmental selection (deterministic processes) and spatial factors (stochastic processes) seemed to determine the assembly and biogeography of habitat generalists. However, for specialists, deterministic processes strongly influenced the distribution, while stochastic processes were not at play. Environmental drivers for generalists and specialists differed, as did their importance. Elevation, total nitrogen and pH were the main factors determining habitat generalists, and soil water content, nitrate nitrogen and pH had the strongest impacts on specialists. Moreover, variation partitioning analysis revealed that environmental selection had a much greater impact on both generalists (17.7% of pure variance was explained) and specialists (3.6%) than spatial factors. However, generalists had a much stronger response to spatial factors (2.3%) than specialists (0.3%). More importantly, null models of β-diversity suggested that specialists deviated significantly from non-neutral assembly mechanisms (relative null deviation= 0.64-0.74) relative to generalists (0.16-0.65) (P < 0.05). These results indicate that generalists and specialists are governed by different assembly mechanisms and present distinct biogeographical patterns. The large proportion of unexplained variation in specialists (93.3%) implies that very complex assembly mechanisms exist in the assembly of specialists across elevational gradients on the subalpine slope of Mount Wutai. It is essential to understand the microbial community assembly at a more refined level, and to expand the current understanding of microbial ecological mechanisms.

Project description:Recovery of an ecosystem following disturbance can be severely hampered or even shift altogether when a point disturbance exceeds a certain spatial threshold. Such scale-dependent dynamics may be caused by preemptive competition, but may also result from diminished self-facilitation due to weakened ecosystem engineering. Moreover, disturbance can facilitate colonization by engineering species that alter abiotic conditions in ways that exacerbate stress on the original species. Consequently, establishment of such counteracting engineers might reduce the spatial threshold for the disturbance, by effectively slowing recovery and increasing the risk for ecosystem shifts to alternative states. We tested these predictions in an intertidal mudflat characterized by a two-state mosaic of hummocks (humps exposed during low tide) dominated by the sediment-stabilizing seagrass Zostera noltii) and hollows (low-tide waterlogged depressions dominated by the bioturbating lugworm Arenicola marina). In contrast to expectations, seagrass recolonized both natural and experimental clearings via lateral expansion and seemed unaffected by both clearing size and lugworm addition. Near the end of the growth season, however, an additional disturbance (most likely waterfowl grazing and/or strong hydrodynamics) selectively impacted recolonizing seagrass in the largest (1 m(2)) clearings (regardless of lugworm addition), and in those medium (0.25 m(2)) clearings where lugworms had been added nearly five months earlier. Further analyses showed that the risk for the disturbance increased with hollow size, with a threshold of 0.24 m(2). Hollows of that size were caused by seagrass removal alone in the largest clearings, and by a weaker seagrass removal effect exacerbated by lugworm bioturbation in the medium clearings. Consequently, a sufficiently large disturbance increased the vulnerability of recolonizing seagrass to additional disturbance by weakening seagrass engineering effects (sediment stabilization). Meanwhile, the counteracting ecosystem engineering (lugworm bioturbation) reduced that threshold size. Therefore, scale-dependent interactions between habitat-mediated facilitation, competition and disturbance seem to maintain the spatial two-state mosaic in this ecosystem.

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

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