Oligotyping: differentiating between closely related microbial taxa using 16S <scp>rRNA</scp> gene data

Eren, A. Murat; Maignien, Loïs; Sul, Woo Jun; Murphy, Leslie G.; Grim, Sharon L.; Morrison, Hilary G.; Sogin, Mitchell L.

doi:10.1111/2041-210x.12114

Cited by 578 publications

(632 citation statements)

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“…The phylogenetic tree, which was used for unweighted and weighted UniFrac analyses, was constructed in QIIME 1.8 using RAxML (Stamatakis et al, 2005). Because 97% OTU clusters can mask important within and between sample diversity (Eren et al, 2013;Sanders et al, 2014), we further examined genotype/strain variation within 97% OTUs among sampling sites and treatments (see Supplementary Text for analysis).…”

Section: Discussionmentioning

confidence: 99%

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

et al. 2015

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Diverse microbial consortia profoundly influence animal biology, necessitating an understanding of microbiome variation in studies of animal adaptation. Yet, little is known about such variability among fish, in spite of their importance in aquatic ecosystems. The Trinidadian guppy, Poecilia reticulata, is an intriguing candidate to test microbiome-related hypotheses on the drivers and consequences of animal adaptation, given the recent parallel origins of a similar ecotype across streams. To assess the relationships between the microbiome and host adaptation, we used 16S rRNA amplicon sequencing to characterize gut bacteria of two guppy ecotypes with known divergence in diet, life history, physiology and morphology collected from low-predation (LP) and high-predation (HP) habitats in four Trinidadian streams. Guts were populated by several recurring, core bacteria that are related to other fish associates and rarely detected in the environment. Although gut communities of lab-reared guppies differed from those in the wild, microbiome divergence between ecotypes from the same stream was evident under identical rearing conditions, suggesting host genetic divergence can affect associations with gut bacteria. In the field, gut communities varied over time, across streams and between ecotypes in a stream-specific manner. This latter finding, along with PICRUSt predictions of metagenome function, argues against strong parallelism of the gut microbiome in association with LP ecotype evolution. Thus, bacteria cannot be invoked in facilitating the heightened reliance of LP guppies on lower-quality diets. We argue that the macroevolutionary microbiome convergence seen across animals with similar diets may be a signature of secondary microbial shifts arising some time after host-driven adaptation.

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Section: Discussionmentioning

confidence: 99%

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

et al. 2015

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“…Spearman's rank correlation coefficient ρ for each oligotype distribution and environmental parameter, and Storey's false discovery rate correction for multiple tests at qo0.05 showed significant (Po0.05) correlations. As oligotyping resolves subtle variations of 16S rRNA genes that represent distinct ecotypes (Ward, 1998;Eren et al, 2013), we argue that oligotypes that correlate significantly with environmental parameters likely represent distinct ecotypes. The relative abundances of six Colwellia oligotypes (types_01, 02, 03, 04, 06, 09), three Cycloclasticus oligotypes (types_04, 06, 30) and one Oceaniserpentilla oligotype (type_17) strongly tracked the elevated methane concentrations in the deepwater hydrocarbon plume; these same samples also had high concentrations of colored dissolved organic matter, a good proxy for dissolved oil (Wade et al, 2013;Supplementary Table S5).…”

Section: Environmental Factors Driving Oligotype Distribution and Abumentioning

confidence: 94%

“…Instead, oligotypes had differential appearance patterns, which cannot be explained by the presence of multiple gene copies. Thus, oligotyping enhances the interpretation of 16S rRNA gene sequence diversity, enabling quantification of ecologically relevant changes in microbial populations at the level of specific ecotypes (Ward, 1998;Eren et al, 2013). We resolved 21 Oceaniserpentilla oligotypes (representing 97.4% of all reads in that genus), 31 Cycloclasticus oligotypes (92.4%) and 26 Colwellia oligotypes (94%).…”

Section: Oligotype Diversity Among Key Hydrocarbon Degradersmentioning

confidence: 99%

“…The common approach of 16S ribosomal RNA (rRNA) gene sequence taxon assignments typically relies on sequence similarity thresholds (for example, 97%) to identify operational taxonomic units (OTUs), aiming to minimize the influence of random sequencing errors (Huse et al, 2010;Kunin et al, 2010). Although distribution patterns of OTUs among environmental samples are frequently used to infer ecological functions of microbial populations, this approach does not detect small variations in the 16S rRNA gene sequence that reflects different ecotypes (Ward, 1998;Eren et al, 2013). The ecotype concept describes a collection of strains with subtly different genetic elements, which afford the ability to occupy slightly different ecological niches while preserving the genetic signature and the (nearly) full ecophysiological potential (Konstantinidis and Tiedje, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume

et al. 2015

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The Deepwater Horizon (DWH) oil well blowout generated an enormous plume of dispersed hydrocarbons that substantially altered the Gulf of Mexico's deep-sea microbial community. A significant enrichment of distinct microbial populations was observed, yet, little is known about the abundance and richness of specific microbial ecotypes involved in gas, oil and dispersant biodegradation in the wake of oil spills. Here, we document a previously unrecognized diversity of closely related taxa affiliating with Cycloclasticus, Colwellia and Oceanospirillaceae and describe their spatio-temporal distribution in the Gulf's deepwater, in close proximity to the discharge site and at increasing distance from it, before, during and after the discharge. A highly sensitive, computational method (oligotyping) applied to a data set generated from 454-tag pyrosequencing of bacterial 16S ribosomal RNA gene V4-V6 regions, enabled the detection of population dynamics at the sub-operational taxonomic unit level (0.2% sequence similarity). The biogeochemical signature of the deep-sea samples was assessed via total cell counts, concentrations of short-chain alkanes (C 1 -C 5 ), nutrients, (colored) dissolved organic and inorganic carbon, as well as methane oxidation rates. Statistical analysis elucidated environmental factors that shaped ecologically relevant dynamics of oligotypes, which likely represent distinct ecotypes. Major hydrocarbon degraders, adapted to the slow-diffusive natural hydrocarbon seepage in the Gulf of Mexico, appeared unable to cope with the conditions encountered during the DWH spill or were outcompeted. In contrast, diverse, rare taxa increased rapidly in abundance, underscoring the importance of specialized subpopulations and potential ecotypes during massive deep-sea oil discharges and perhaps other large-scale perturbations.

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“…The oligotyping computational method (Eren et al, 2011(Eren et al, , 2013a further explored potential host-specificity patterns using subtle nucleotide variation in closely related Hexadella microbiota. From the entire data set, we submitted 2 112 927 high-quality Illumina V6 fragments that GAST identified as Nitrospira to the oligotyping pipeline version 0.6 (available from http://oligotyping.org).…”

Section: Oligotypingmentioning

confidence: 99%

Host-specificity among abundant and rare taxa in the sponge microbiome

Réveillaud¹,

Maignien²,

Eren³

et al. 2014

The ISME Journal

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Microbial communities have a key role in the physiology of the sponge host, and it is therefore essential to understand the stability and specificity of sponge-symbiont associations. Host-specific bacterial associations spanning large geographic distance are widely acknowledged in sponges. However, the full spectrum of specificity remains unclear. In particular, it is not known whether closely related sponges host similar or very different microbiota over wide bathymetric and geographic gradients, and whether specific associations extend to the rare members of the sponge microbiome. Using the ultra-deep Illumina sequencing technology, we conducted a comparison of sponge bacterial communities in seven closely related Hexadella species with a well-resolved host phylogeny, as well as of a distantly related sponge Mycale. These samples spanned unprecedentedly large bathymetric (15-960 m) gradients and varying European locations. In addition, this study included a bacterial community analysis of the local background seawater for both Mycale and the widespread deep-sea taxa Hexadella cf. dedritifera. We observed a striking diversity of microbes associated with the sponges, spanning 47 bacterial phyla. The data did not reveal any Hexadella microbiota co-speciation pattern, but confirmed sponge-specific and species-specific host-bacteria associations, even within extremely low abundant taxa. Oligotyping analysis also revealed differential enrichment preferences of closely related Nitrospira members in closely related sponges species. Overall, these results demonstrate highly diverse, remarkably specific and stable spongebacteria associations that extend to members of the rare biosphere at a very fine phylogenetic scale, over significant geographic and bathymetric gradients.

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Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data

Cited by 578 publications

References 56 publications

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

Diverse, rare microbial taxa responded to the Deepwater Horizon deep-sea hydrocarbon plume

Host-specificity among abundant and rare taxa in the sponge microbiome

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