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Microbiome niche modification drives diurnal rumen community assembly, overpowering individual variability and diet effects.

ABSTRACT: Niche modification is a process whereby the activity of organisms modifies their local environment creating new niches for other organisms. This process can have a substantial role in community assembly of gut microbial ecosystems due to their vast and complex metabolic activities. We studied the postprandial diurnal community oscillatory patterns of the rumen microbiome and showed that metabolites produced by the rumen microbiome condition its environment and lead to dramatic diurnal changes in community composition and function. After feeding, microbiome composition undergoes considerable change in its phylogenetic breadth manifested as a significant 3-5-fold change in the relative abundance of methanogenic archaea and main bacterial taxa such as Prevotella, in a manner that was independent of individual host variation and diet. These changes in community composition were accompanied by changes in pH and methane partial pressure, suggesting a strong functional connection. Notably, cross-incubation experiments combining metabolites and organisms from different diurnal time points showed that the metabolites released by microbes are sufficient to reproduce changes in community function comparable to those observed in vivo. These findings highlight microbiome niche modification as a deterministic process that drives diurnal community assembly via environmental filtering.

SUBMITTER: Shaani Y

PROVIDER: S-EPMC6154959 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Sulfate-reducing bacteria (SRB) are essential functional microbial taxa for degrading organic matter (OM) in anoxic marine environments. However, there are little experimental data regarding how SRB regulates microbial communities. Here, we applied a top-down microbial community management approach by inhibiting SRB to elucidate their contributions to the microbial community during OM degradation. Based on the highly replicated microcosms (n = 20) of five different incubation stages, we found that many microbial community properties were influenced after inhibiting SRB, including the composition, structure, network, and community assembly processes. We also found a strong coexistence pattern between SRB and other abundant phylogenetic lineages via positive frequency-dependent selection. The relative abundances of the families Synergistaceae, Peptostreptococcaceae, Dethiosulfatibacteraceae, Prolixibacteraceae, Marinilabiliaceae, and Marinifilaceae were simultaneously suppressed after inhibiting SRB during OM degradation. A close association between SRB and the order Marinilabiliales among coexisting taxa was most prominent. They contributed to preserved modules during network successions, were keystone nodes mediating the networked community, and contributed to homogeneous ecological selection. The molybdate tolerance test of the isolated strains of Marinilabiliales showed that inhibited SRB (not the inhibitor of SRB itself) triggered a decrease in the relative abundance of Marinilabiliales. We also found that inhibiting SRB resulted in reduced pH, which is unsuitable for the growth of most Marinilabiliales strains, while the addition of pH buffer (HEPES) in SRB-inhibited treatment microcosms restored the pH and the relative abundances of these bacteria. These data supported that SRB could modify niches to affect species coexistence. IMPORTANCE Our model offers insight into the ecological properties of SRB and identifies a previously undocumented dimension of OM degradation. This targeted inhibition approach could provide a novel framework for illustrating how functional microbial taxa associate the composition and structure of the microbial community, molecular ecological network, and community assembly processes. These findings emphasize the importance of SRB during OM degradation. Our results proved the feasibility of the proposed study framework, inhibiting functional taxa at the community level, for illustrating when and to what extent functional taxa can contribute to ecosystem services.

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Microbiome niche modification drives diurnal rumen community assembly, overpowering individual variability and diet effects.

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