Dataset Information

Rare Taxa Exhibit Disproportionate Cell-Level Metabolic Activity in Enriched Anaerobic Digestion Microbial Communities.

ABSTRACT: Microbial communities are composed of populations with vastly different abundances and levels of metabolic and replicative activity, ranging from actively metabolizing and dividing to dormant or nonviable. The 16S rRNA/rDNA ratio is an emerging tool for evaluating cell-level metabolic activity independent of abundance. In this study, we used five long-term enriched model anaerobic digestion (AD) communities to investigate community composition, diversity, structure, and in particular activity based on the rRNA/rDNA ratio. We cross-validated the 16S amplicon-based results using two alternative operational taxonomic unit (OTU) formation methods (conventional 97% sequence similarity and 100% sequence similar zero-radius OTUs by UNOISE3) and compared these to metagenome-derived population genomes and metatranscriptomes. Significant positive correlations were observed between microbial total activity and abundance with both the amplicon- and omic-based methods. All three methods revealed disproportionately high transcription/abundance ratios for some rare taxa but lower ratios for most abundant taxa for all the communities, which was further corroborated by the high replication rate (iRep) of most low-abundance population genomes. IMPORTANCE Variation in microbial activity levels is increasingly being recognized as both an important dimension in community function and a complicating factor in sequencing-based survey methods. This study extends previous reports that rare taxa may contribute disproportionately to community activity in some natural environments, showing that this may also hold in artificially maintained model communities with well-described inputs, outputs, and biochemical functions. These results demonstrate that assessment of activity levels using the rRNA/rDNA ratio is robust across taxonomic unit formation methods and is independently corroborated by omics methods. The results also provide insight into the comparative advantages and disadvantages of different taxonomic unit formation methods in amplicon sequencing studies, showing that UNOISE3 provides comparable microbial diversity, structure, and activity information as the 97% sequence similarity method but potentially loses some phylogenetic diversity and creates more "phantom taxa" (which are present in the RNA pool but not the corresponding DNA pool).

SUBMITTER: Jia Y

PROVIDER: S-EPMC6343076 | biostudies-literature | 2019 Jan-Feb

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Rare Taxa Exhibit Disproportionate Cell-Level Metabolic Activity in Enriched Anaerobic Digestion Microbial Communities.

Jia Yangyang Y Leung Marcus H Y MHY Tong Xinzhao X Wilkins David D Lee Patrick K H PKH

mSystems 20190122 1

Microbial communities are composed of populations with vastly different abundances and levels of metabolic and replicative activity, ranging from actively metabolizing and dividing to dormant or nonviable. The 16S rRNA/rDNA ratio is an emerging tool for evaluating cell-level metabolic activity independent of abundance. In this study, we used five long-term enriched model anaerobic digestion (AD) communities to investigate community composition, diversity, structure, and in particular activity ba ...[more]

PMID: 30687779

Similar Datasets

Project description:Background:Anaerobic digestion, whose final products are methane and carbon dioxide, ensures energy flow and circulation of matter in ecosystems. This naturally occurring process is used for the production of renewable energy from biomass. Lactate, a common product of acidic fermentation, is a key intermediate in anaerobic digestion of biomass in the environment and biogas plants. Effective utilization of lactate has been observed in many experimental approaches used to study anaerobic digestion. Interestingly, anaerobic lactate oxidation and lactate oxidizers as a physiological group in methane-yielding microbial communities have not received enough attention in the context of the acetogenic step of anaerobic digestion. This study focuses on metabolic transformation of lactate during the acetogenic and methanogenic steps of anaerobic digestion in methane-yielding bioreactors. Results:Methane-yielding microbial communities instead of pure cultures of acetate producers were used to process artificial lactate-rich media to methane and carbon dioxide in up-flow anaerobic sludge blanket reactors. The media imitated the mixture of acidic products found in anaerobic environments/digesters where lactate fermentation dominates in acidogenesis. Effective utilization of lactate and biogas production was observed. 16S rRNA profiling was used to examine the selected methane-yielding communities. Among Archaea present in the bioreactors, the order Methanosarcinales predominated. The acetoclastic pathway of methane formation was further confirmed by analysis of the stable carbon isotope composition of methane and carbon dioxide. The domain Bacteria was represented by Bacteroidetes, Firmicutes, Proteobacteria, Synergistetes, Actinobacteria, Spirochaetes, Tenericutes, Caldithrix, Verrucomicrobia, Thermotogae, Chloroflexi, Nitrospirae, and Cyanobacteria. Available genome sequences of species and/or genera identified in the microbial communities were searched for genes encoding the lactate-oxidizing metabolic machinery homologous to those of Acetobacterium woodii and Desulfovibrio vulgaris. Furthermore, genes for enzymes of the reductive acetyl-CoA pathway were present in the microbial communities. Conclusions:The results indicate that lactate is oxidized mainly to acetate during the acetogenic step of AD and this comprises the acetotrophic pathway of methanogenesis. The genes for lactate utilization under anaerobic conditions are widespread in the domain Bacteria. Lactate oxidation to the substrates for methanogens is the most energetically attractive process in comparison to butyrate, propionate, or ethanol oxidation.

Project description:BACKGROUND:The species composition of a microbial community is rarely fixed and often experiences fluctuations of varying degrees and at varying frequencies. These perturbations to a community's taxonomic profile naturally also alter the community's functional profile-the aggregate set of genes encoded by community members-ultimately altering the community's overall functional capacities. The magnitude of such functional changes and the specific shift that will occur in each function, however, are strongly dependent on how genes are distributed across community members' genomes. This gene distribution, in turn, is determined by the taxonomic composition of the community and would markedly differ, for example, between communities composed of species with similar genomic content vs. communities composed of species whose genomes encode relatively distinct gene sets. Combined, these observations suggest that community functional robustness to taxonomic perturbations could vary widely across communities with different compositions, yet, to date, a systematic study of the inherent link between community composition and robustness is lacking. RESULTS:In this study, we examined how a community's taxonomic composition influences the robustness of that community's functional profile to taxonomic perturbation (here termed taxa-function robustness) across a wide array of environments. Using a novel simulation-based computational model to quantify this taxa-function robustness in host-associated and non-host-associated communities, we find notable differences in robustness between communities inhabiting different body sites, including significantly higher robustness in gut communities compared to vaginal communities that cannot be attributed solely to differences in species richness. We additionally find between-site differences in the robustness of specific functions, some of which are potentially related to site-specific environmental conditions. These taxa-function robustness differences are most strongly associated with differences in overall functional redundancy, though other aspects of gene distribution also influence taxa-function robustness in certain body environments, and are sufficient to cluster communities by environment. Further analysis revealed a correspondence between our robustness estimates and taxonomic and functional shifts observed across human-associated communities. CONCLUSIONS:Our analysis approach revealed intriguing taxa-function robustness variation across environments and identified features of community and gene distribution that impact robustness. This approach could be further applied for estimating taxa-function robustness in novel communities and for informing the design of synthetic communities with specific robustness requirements.

Project description:Recent studies evaluating the community structures of microorganisms and macroorganisms have found greater diversity and rarity within micro-scale communities, compared to macro-scale communities. However, reproductive method has been a confounding factor in these comparisons; the microbes considered generally reproduce asexually, while the macroorganisms considered generally reproduce sexually. Sexual reproduction imposes the constraint of mate finding, which can have significant demographic consequences by depressing birth rates at low population sizes. First, I construct an island biogeography model to study the organization of ecological communities under neutral stochastic processes. Then, I examine theoretically how the effects of mate finding in sexual populations translate to the emergent community properties of diversity, rarity, and dominance (size of the largest population). In mate-limited sexual populations, the decreased growth rates at low population densities translate to a higher extinction rate; this increased extinction rate had a disproportionately strong effect on taxa with low population densities. Thus, mate limitation decreased diversity, primarily by excluding small populations from communities. However, the most abundant taxa were minimally affected by mate limitation. Therefore, mate limitation affected the diversity and rarity of taxa in communities but did not alter the dominance of the largest population. The observed shifts in community structure mirror recent empirical studies of micro-scale versus macro-scale communities, which have shown that microbial communities have greater diversity and rarity than macrobial communities but are not different in dominance. Thus, reproductive method may contribute to observed differences in emergent properties between communities at these two scales.IMPORTANCE There have been numerous recent efforts to integrate microbes into broad-scale ecological theories. Microbial communities are often structurally distinct from macrobial communities, but it is unclear whether these differences are real or whether they are due to the different methodologies used to study communities at these two scales. One major difference between macroorganisms and microorganisms is that microbes are much more likely to reproduce asexually. Sexually reproducing taxa have diminished growth rates at low population size, because they must encounter another member of their species before reproducing. This study shows that communities of asexually reproducing taxa are expected to be more diverse, because taxa persist longer. Furthermore, asexually reproducing taxa can exist at much lower densities than sexually reproducing taxa. Thus, asexual reproduction by microbes can account for two major differences between microbial and macrobial communities, namely, greater diversity and greater prevalence of rare taxa for microbes.

Dataset Information

Rare Taxa Exhibit Disproportionate Cell-Level Metabolic Activity in Enriched Anaerobic Digestion Microbial Communities.

Publications

Rare Taxa Exhibit Disproportionate Cell-Level Metabolic Activity in Enriched Anaerobic Digestion Microbial Communities.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets