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Asexual Reproduction Can Account for the High Diversity and Prevalence of Rare Taxa Observed in Microbial Communities.

ABSTRACT: 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.

SUBMITTER: Herren CM

PROVIDER: S-EPMC6643231 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Asexual Reproduction Can Account for the High Diversity and Prevalence of Rare Taxa Observed in Microbial Communities.

Herren Cristina M CM

Applied and environmental microbiology 20190718 15

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 co ...[more]

PMID: 31126951

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Project description:Microbial communities typically contain many rare taxa that make up the majority of the observed membership, yet the contribution of this microbial "rare biosphere" to community dynamics is unclear. Using 16S rRNA amplicon sequencing of 3,237 samples from 42 time series of microbial communities from nine different ecosystems (air; marine; lake; stream; adult human skin, tongue, and gut; infant gut; and brewery wastewater treatment), we introduce a new method to detect typically rare microbial taxa that occasionally become very abundant (conditionally rare taxa [CRT]) and then quantify their contributions to temporal shifts in community structure. We discovered that CRT made up 1.5 to 28% of the community membership, represented a broad diversity of bacterial and archaeal lineages, and explained large amounts of temporal community dissimilarity (i.e., up to 97% of Bray-Curtis dissimilarity). Most of the CRT were detected at multiple time points, though we also identified "one-hit wonder" CRT that were observed at only one time point. Using a case study from a temperate lake, we gained additional insights into the ecology of CRT by comparing routine community time series to large disturbance events. Our results reveal that many rare taxa contribute a greater amount to microbial community dynamics than is apparent from their low proportional abundances. This observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time. Importance: Microbial communities and their processes are the foundations of ecosystems. The ecological roles of rare microorganisms are largely unknown, but it is thought that they contribute to community stability by acting as a reservoir that can rapidly respond to environmental changes. We investigated the occurrence of typically rare taxa that very occasionally become more prominent in their communities ("conditionally rare"). We quantified conditionally rare taxa in time series from a wide variety of ecosystems and discovered that not only were conditionally rare taxa present in all of the examples, but they also contributed disproportionately to temporal changes in diversity when they were most abundant. This result indicates an important and general role for rare microbial taxa within their communities.

Project description: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).

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Project description:A global phenomenon of increasing bark beetle-induced tree mortality has heightened concern regarding ecosystem response and biogeochemical implications. Here we explore microbial dynamics under lodgepole pines through the analysis of bulk (16S rDNA) and potentially active (16S rRNA) communities to understand terrestrial ecosystem responses associated with this form of large-scale tree morality. We found that the relative abundance of bulk and potentially active taxa was correlated across taxonomic levels, but at lower levels cladal differences became more apparent. Despite this correlation, there was a strong differentiation of community composition between bulk and potentially active taxa, with further clustering in association with stages of tree mortality. Surprisingly, community clustering as a function of tree phase had limited correlation to soil water content and total nitrogen concentrations, which were the only two measured edaphic parameters to differ in association with tree phase. Bacterial clustering is more readily explained by the observed decrease in abundance of active, rare microorganisms after tree death in conjunction with stable alpha diversity measurements. This enables the rare fraction of the terrestrial microbial community to maintain metabolic diversity by transitioning between metabolically active and dormant states during this ecosystem disturbance and contributes disproportionately to community dynamics and archived metabolic capabilities. These results suggest that analyzing the bulk and potentially active communities after beetle infestation might be a more sensitive indicator of disruption than measuring local edaphic parameters.ImportanceForests around the world are experiencing unprecedented mortality due to insect infestations fueled in part by a changing climate. While above-ground processes have been explored, changes at the terrestrial interface relevant to microbial biogeochemical cycling remain largely unknown. In this study, we investigated the changing bulk and potentially active microbial communities beneath healthy and beetle-killed trees. We found that even though few edaphic parameters were altered from beetle infestation, the rare microbes were more likely to be active and fluctuate between dormancy and metabolic activity. This indicates rare as opposed to abundant taxa contribute disproportionately to microbial community dynamics and presumably biogeochemical cycling within these types of perturbed ecosystems.

Project description:BackgroundIncreasing studies have demonstrated potential disproportionate functional and ecological contributions of rare taxa in a microbial community. However, the study of the microbial rare biosphere is hampered by their inherent scarcity and the deficiency of currently available techniques. Sample-wise cross contaminations might be introduced by sample index misassignment in the most widely used metabarcoding amplicon sequencing approach. Although downstream bioinformatic quality control and clustering or denoising algorithms could remove sequencing errors and non-biological artifact reads, no algorithm could eliminate high quality reads from sample-wise cross contaminations introduced by index misassignment, making it difficult to distinguish between bona fide rare taxa and potential false positives in metabarcoding studies.ResultsWe thoroughly evaluated the rate of index misassignment of the widely used NovaSeq 6000 and DNBSEQ-G400 sequencing platforms using both commercial and customized mock communities, and observed significant lower (0.08% vs. 5.68%) fraction of potential false positive reads for DNBSEQ-G400 as compared to NovaSeq 6000. Significant batch effects could be caused by stochastically introduced false positive or false negative rare taxa. These false detections could also lead to inflated alpha diversity of relatively simple microbial communities and underestimated that of complex ones. Further test using a set of cow rumen samples reported differential rare taxa by different sequencing platforms. Correlation analysis of the rare taxa detected by each sequencing platform demonstrated that the rare taxa identified by DNBSEQ-G400 platform had a much higher possibility to be correlated with the physiochemical properties of rumen fluid as compared to NovaSeq 6000 platform. Community assembly mechanism and microbial network correlation analysis indicated that false positive or negative rare taxa detection could lead to biased community assembly mechanism and identification of fake keystone species of the community.ConclusionsWe highly suggest proper positive/negative/blank controls, technical replicate settings, and proper sequencing platform selection in future amplicon studies, especially when the microbial rare biosphere would be focused.

Dataset Information

Asexual Reproduction Can Account for the High Diversity and Prevalence of Rare Taxa Observed in Microbial Communities.

Publications

Asexual Reproduction Can Account for the High Diversity and Prevalence of Rare Taxa Observed in Microbial Communities.

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