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Description: Background The increasing availability of microbial genomes and environmental shotgun metagenomes provides unprecedented access to the genomic differences within related bacteria. The human oral microbiome with its diverse habitats and abundant, relatively well-characterized microbial inhabitants presents an opportunity to investigate bacterial population structures at an ecosystem scale. Results Here, we employ a metapangenomic approach that combines public genomes with Human Microbiome Project (HMP) metagenomes to study the diversity of microbial residents of three oral habitats: tongue dorsum, buccal mucosa, and supragingival plaque. For two exemplar taxa, Haemophilus parainfluenzae and the genus Rothia, metapangenomes reveal distinct genomic groups based on shared genome content. H. parainfluenzae genomes separate into three distinct subgroups with differential abundance between oral habitats. Functional enrichment analyses identify an operon encoding oxaloacetate decarboxylase as diagnostic for the tongue-abundant subgroup. For the genus Rothia, grouping by shared genome content recapitulates species-level taxonomy and habitat preferences. However, while most R. mucilaginosa are restricted to the tongue as expected, two genomes represent a cryptic population of R. mucilaginosa in many buccal mucosa samples. For both H. parainfluenzae and the genus Rothia, we identify not only limitations in the ability of cultivated organisms to represent populations in their native environment, but also specifically which cultivar gene sequences are absent or ubiquitous. Conclusions Our findings provide insights into population structure and biogeography in the mouth and form specific hypotheses about habitat adaptation. These results illustrate the power of combining metagenomes and pangenomes to investigate the ecology and evolution of bacteria across analytical scales.

Print ISSN: 1465-6906

Electronic ISSN: 1474-760X

Topics: Biology

Published by BioMed Central

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Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments (2021)

Gomaa, Fatma ; Utter, Daniel R. ; Powers, Christopher ; [et al.]

American Association for the Advancement of Science

In: Science Advances. 2021; 7(22): Published 2021 May 01. doi: 10.1126/sciadv.abf1586.

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Publication Date: 2021-05-01

Electronic ISSN: 2375-2548

Topics: Natural Sciences in General

Published by American Association for the Advancement of Science

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A few Pseudomonas oligotypes dominate in the meat and dairy processing environment (2017)

Stellato, Giuseppina ; Utter, Daniel R. ; Voorhis, Andy ; [et al.]

Frontiers Media

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Publication Date: 2022-05-25

Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 8 (2017): 264, doi:10.3389/fmicb.2017.00264.

Description: The occurrence of bacteria in the food processing environments plays a key role in food contamination and development of spoilage. Species of the genus Pseudomonas are recognized as major food spoilers and the capability to actually determine spoilage can be species- as well as strain-dependent. In order to improve the taxonomic resolution of 16S rRNA gene amplicons, in this study we used oligotyping to investigate the diversity of Pseudomonas populations in meat and dairy processing environments. Sequences of the V1–V3 regions from previous studies were used, including environmental swabs and food samples from both meat and dairy processing plants. We showed that the most frequently found oligotypes belonged to Pseudomonas fragi and P. fluorescens, that the most abundant oligotypes co-occurred, and were shared between the meat and dairy datasets. All the oligotypes occurring in foods were also identified in the environmental samples of the corresponding plants, highlighting the important role of the environment as a source of strains for food contamination. Oligotypes of the same species showed different levels depending on food processing and type of sample, suggesting that different strains of the same species can have different adaptation efficiency, leading to resilient bacterial associations.

Keywords: Pseudomonas fragi ; Food contamination ; Food processing environment ; Oligotyping ; 16S rRNA gene sequencing

Repository Name: Woods Hole Open Access Server

Type: Article

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Individuality, stability, and variability of the plaque microbiome (2016)

Utter, Daniel R. ; Mark Welch, Jessica L. ; Borisy, Gary G.

Frontiers Media

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Publication Date: 2022-05-26

Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Microbiology 7 (2016): 564, doi:10.3389/fmicb.2016.00564.

Description: Dental plaque is a bacterial biofilm composed of a characteristic set of organisms. Relatively little information from cultivation-independent, high-throughput analyses has been published on the temporal dynamics of the dental plaque microbiome. We used Minimum Entropy Decomposition, an information theory-based approach similar to oligotyping that provides single-nucleotide resolution, to analyze a previously published time series data set and investigate the dynamics of the plaque microbiome at various analytic and taxonomic levels. At both the genus and 97% Operational Taxonomic Unit (OTU) levels of resolution, the range of variation within each individual overlapped that of other individuals in the data set. When analyzed at the oligotype level, however, the overlap largely disappeared, showing that single-nucleotide resolution enables differentiation of individuals from one another without ambiguity. The overwhelming majority of the plaque community in all samples was made up of bacteria from a moderate number of plaque-typical genera, indicating that the overall community framework is shared among individuals. Each of these genera fluctuated in abundance around a stable mean that varied between individuals, with some genera having higher inter-individual variability than others. Thus, at the genus level, differences between individuals lay not in the identity of the major genera but in consistently differing proportions of these genera from mouth to mouth. However, at the oligotype level, we detected oligotype “fingerprints,” a highly individual-specific set of persistently abundant oligotypes fluctuating around a stable mean over time. For example, within the genus Corynebacterium, more than a dozen oligotypes were detectable in each individual, of which a different subset reached high abundance in any given person. This pattern suggests that each mouth contains a subtly different community of organisms. We also compared the Chinese plaque community characterized here to previously characterized Western plaque communities, as represented by analyses of data emerging from the Human Microbiome Project, and found no major differences between Chinese and Western supragingival plaque. In conclusion, we found the plaque microbiome to be highly individualized at the oligotype level and characterized by stability of community membership, with variability in the relative abundance of community members between individuals and over time.

Description: Our work was supported by National Institutes of Health (NIH) National Institute of Dental and Craniofacial Research Grant DE022586 (to GGB). Additional support was provided by Harvard University's Department of Organismic and Evolutionary Biology graduate program (to DRU).

Keywords: Human microbiome ; 16S rRNA ; Community dynamics ; Oral microbiota ; Community ecology

Repository Name: Woods Hole Open Access Server

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Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments (2021)

Gomaa, Fatma ; Utter, Daniel R. ; Powers, Christopher ; [et al.]

American Association for the Advancement of Science

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Publication Date: 2022-05-27

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Gomaa, F., Utter, D. R., Powers, C., Beaudoin, D. J., Edgcomb, V. P., Filipsson, H. L., Hansel, C. M., Wankel, S. D., Zhang, Y., & Bernhard, J. M. Multiple integrated metabolic strategies allow foraminiferan protists to thrive in anoxic marine sediments. Science Advances, 7(22), (2021): eabf1586, https://doi.org/10.1126/sciadv.abf1586.

Description: Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic sediments identified metabolic strategies used by this abundant taxon. In field-collected and laboratory-incubated samples, foraminifera expressed denitrification genes regardless of oxygen regime with a putative nitric oxide dismutase, a characteristic enzyme of oxygenic denitrification. A pyruvate:ferredoxin oxidoreductase was highly expressed, indicating the capability for anaerobic energy generation during exposure to hypoxia and anoxia. Near-complete expression of a diatom’s plastid genome in one foraminiferal species suggests kleptoplasty or sequestration of functional plastids, conferring a metabolic advantage despite the host living far below the euphotic zone. Through a unique integration of functions largely unrecognized among “typical” eukaryotes, benthic foraminifera represent winning microeukaryotes in the face of ongoing oceanic deoxygenation.

Description: his project was funded by the U.S. NSF IOS 1557430 and 1557566. H.L.F. acknowledges support from the Swedish Research Council VR (grant number 2017-04190).

Repository Name: Woods Hole Open Access Server

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Exploring the protist microbiome: the diversity of bacterial communities associated with Arcella spp. (Tubulina: Amoebozoa) (2022)

Gomaa, Fatma ; Utter, Daniel R. ; Loo, Wesley ; [et al.]

Elsevier

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Publication Date: 2022-08-02

Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Gomaa, F., Utter, D. R., Loo, W., Lahr, D. J. G., & Cavanaugh, C. M. Exploring the protist microbiome: the diversity of bacterial communities associated with Arcella spp. (Tubulina: Amoebozoa). European Journal of Protistology, 82, (2022): 125861, https://doi.org/10.1016/j.ejop.2021.125861.

Description: Research on protist-bacteria interactions is increasingly relevant as these associations are now known to play important roles in ecosystem and human health. Free-living amoebae are abundant in all environments and are frequent hosts for bacterial endosymbionts including pathogenic bacteria. However, to date, only a small fraction of these symbionts have been identified, while the structure and composition of the total symbiotic bacterial communities still remains largely unknown. Here, we use the testate amoeba Arcella spp. as model organisms to investigate the specificity and diversity of Arcella-associated microbial communities. High-throughput amplicon sequencing from the V4 region of the 16S rRNA gene revealed high diversity in the bacterial communities associated with the wild Arcella spp. To investigate the specificity of the associated bacterial community with greater precision, we investigated the bacterial communities of two lab-cultured Arcella species, A. hemispherica and A. intermedia, grown in two different media types. Our results suggest that Arcella-bacteria associations are species-specific, and that the associated bacterial community of lab-cultured Arcella spp. remains distinct from that of the surrounding media. Further, each host Arcella species could be distinguished based on its bacterial composition. Our findings provide insight into the understanding of eukaryotic-bacterial symbiosis.

Description: This project was funded by National Science Foundation Postdoctoral Research Fellowship in Biology to F. Gomaa, Grant Number: PRFB1611514. Support was provided to D.R.U. from the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE1745303 to D.R.U and by Harvard University’s Department of Organismic and Evolutionary Biology program.

Keywords: Arcella- associated microbiome ; Intracellular bacterial diversity ; Heterotrophic amoebae ; Amoeba-resistant bacteria

Repository Name: Woods Hole Open Access Server

Type: Article

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