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Diversity and geochemical community assembly processes of the living rare biosphere in a sand-and-gravel aquifer ecosystem in the Midwestern United States.

ABSTRACT: Natural microbial communities consist of a limited number of abundant species and an extraordinarily diverse population of rare species referred to as the rare biosphere. Recent studies have revealed that the rare biosphere is not merely an inactive dormant population but may play substantial functional roles in the ecosystem. However, structure, activity and community assembly processes of the rare biosphere are poorly understood. In this study, we evaluated the present and living microbial community structures including rare populations in an aquifer ecosystem, the Mahomet Aquifer, USA, by both 16S rDNA and rRNA amplicon deep sequencing. The 13 groundwater samples formed three distinct groups based on the "entire" community structure, and the same grouping was obtained when focusing on the "rare" subcommunities (<0.1% of total abundance), while the "abundant" subcommunities (>1.0%) gave a different grouping. In the correlation analyses, the observed grouping pattern is associated with several geochemical factors, and structures of not only the entire community but also the rare subcommunity are correlated with geochemical profiles in the aquifer ecosystem. Our findings first indicate that the living rare biosphere in the aquifer system has the metabolic potential to adapt to local geochemical factors which dictate the community assembly processes.

SUBMITTER: Yamamoto K

PROVIDER: S-EPMC6748922 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:A single liter of water contains hundreds, if not thousands, of bacterial and archaeal species, each of which typically makes up a very small fraction of the total microbial community (<0.1%), the so-called "rare biosphere." How often, and via what mechanisms, e.g., clonal amplification versus horizontal gene transfer, the rare taxa and genes contribute to microbial community response to environmental perturbations represent important unanswered questions toward better understanding the value and modeling of microbial diversity. We tested whether rare species frequently responded to changing environmental conditions by establishing 20-liter planktonic mesocosms with water from Lake Lanier (Georgia, USA) and perturbing them with organic compounds that are rarely detected in the lake, including 2,4-dichlorophenoxyacetic acid (2,4-D), 4-nitrophenol (4-NP), and caffeine. The populations of the degraders of these compounds were initially below the detection limit of quantitative PCR (qPCR) or metagenomic sequencing methods, but they increased substantially in abundance after perturbation. Sequencing of several degraders (isolates) and time-series metagenomic data sets revealed distinct cooccurring alleles of degradation genes, frequently carried on transmissible plasmids, especially for the 2,4-D mesocosms, and distinct species dominating the post-enrichment microbial communities from each replicated mesocosm. This diversity of species and genes also underlies distinct degradation profiles among replicated mesocosms. Collectively, these results supported the hypothesis that the rare biosphere can serve as a genetic reservoir, which can be frequently missed by metagenomics but enables community response to changing environmental conditions caused by organic pollutants, and they provided insights into the size of the pool of rare genes and species.IMPORTANCE A single liter of water or gram of soil contains hundreds of low-abundance bacterial and archaeal species, the so called rare biosphere. The value of this astonishing biodiversity for ecosystem functioning remains poorly understood, primarily due to the fact that microbial community analysis frequently focuses on abundant organisms. Using a combination of culture-dependent and culture-independent (metagenomics) techniques, we showed that rare taxa and genes commonly contribute to the microbial community response to organic pollutants. Our findings should have implications for future studies that aim to study the role of rare species in environmental processes, including environmental bioremediation efforts of oil spills or other contaminants.

Project description:BackgroundThe adaptation of pyrosequencing technologies for use in culture-independent diversity surveys allowed for deeper sampling of ecosystems of interest. One extremely well suited area of interest for pyrosequencing-based diversity surveys that has received surprisingly little attention so far, is examining fine scale (e.g. micrometer to millimeter) beta diversity in complex microbial ecosystems.Methodology/principal findingsWe examined the patterns of fine scale Beta diversity in four adjacent sediment samples (1mm apart) from the source of an anaerobic sulfide and sulfur rich spring (Zodletone spring) in southwestern Oklahoma, USA. Using pyrosequencing, a total of 292,130 16S rRNA gene sequences were obtained. The beta diversity patterns within the four datasets were examined using various qualitative and quantitative similarity indices. Low levels of Beta diversity (high similarity indices) were observed between the four samples at the phylum-level. However, at a putative species (OTU(0.03)) level, higher levels of beta diversity (lower similarity indices) were observed. Further examination of beta diversity patterns within dominant and rare members of the community indicated that at the putative species level, beta diversity is much higher within rare members of the community. Finally, sub-classification of rare members of Zodletone spring community based on patterns of novelty and uniqueness, and further examination of fine scale beta diversity of each of these subgroups indicated that members of the community that are unique, but non novel showed the highest beta diversity within these subgroups of the rare biosphere.Conclusions/significanceThe results demonstrate the occurrence of high inter-sample diversity within seemingly identical samples from a complex habitat. We reason that such unexpected diversity should be taken into consideration when exploring gamma diversity of various ecosystems, as well as planning for sequencing-intensive metagenomic surveys of highly complex ecosystems.

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Diversity and geochemical community assembly processes of the living rare biosphere in a sand-and-gravel aquifer ecosystem in the Midwestern United States.

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