Anatomy promotes neutral coexistence of strains in the human skin microbiome

Conwill, Arolyn; Kuan, Anne C.; Damerla, Ravalika; Poret, Alexandra J; Baker, Jacob S; Tripp, A Delphine; Alm, Eric J.; Lieberman, Tami D.

doi:10.1016/j.chom.2021.12.007

Cited by 93 publications

(87 citation statements)

References 95 publications

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“…The structure-induced stability supports the view that community assembly from potential colonizers is shaped by priority effects; whoever invades first enjoys colonization resistance against late invaders. The randomness induced by the order of strain arrival might contribute to the substantial host-to-host variability seen in some host-associated microbial communities ( 9 , 16 ).…”

Section: Discussionmentioning

confidence: 99%

“…The ubiquity of microhabitat-associated stability and colonization resistance raises the question of whether these features generically emerge in confined spaces, for example, soil pores ( 13 – 15 ), skin follicles ( 4 , 16 ), or crypts and folds in gut-like environments ( 5 , 17 , 18 ). Previous studies have identified biological features, such as suppressed biofilm growth or the expression of specific adhesion molecules, that promote stability in specific systems ( 1 , 7 , 19 – 21 ).…”

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confidence: 99%

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Scale-dependent tipping points of bacterial colonization resistance

Karita¹,

Limmer²,

Hallatschek³

2022

Proc. Natl. Acad. Sci. U.S.A.

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Bacteria are efficient colonizers of a wide range of secluded microhabitats, such as soil pores, skin follicles, or intestinal crypts. How the structural diversity of these habitats modulates microbial self-organization remains poorly understood, in part because of the difficulty to precisely manipulate the physical structure of microbial environments. Using a microfluidic device to grow bacteria in crypt-like incubation chambers of systematically varied lengths, we show that small variations in the physical structure of the microhabitat can drastically alter bacterial colonization success and resistance against invaders. Small crypts are uncolonizable; intermediately sized crypts can stably support dilute populations, while beyond a second critical length scale, populations phase separate into a dilute region and a jammed region. The jammed state is characterized by extreme colonization resistance, even if the resident strain is suppressed by an antibiotic. Combined with a flexible biophysical model, we demonstrate that colonization resistance and associated priority effects can be explained by a crowding-induced phase transition, which results from a competition between proliferation and density-dependent cell leakage. The emerging sensitivity to scale underscores the need to control for scale in microbial ecology experiments. Systematic flow-adjustable length-scale variations may serve as a promising strategy to elucidate further scale-sensitive tipping points and to rationally modulate the stability and resilience of microbial colonizers.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Scale-dependent tipping points of bacterial colonization resistance

Karita¹,

Limmer²,

Hallatschek³

2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Importance of host anatomy and spatial structure of microbial communities is recognised in vertebrate microbiome, emphasising the effects of spatiotemporal microbiome variability from skin or gastrointestinal tract down to individual skin pores or even crypts of Lieberkühn (Conwill et al . 2022 and references therein).…”

Section: Discussionmentioning

confidence: 99%

More than just hitchhikers: a survey of bacterial communities associated with diatoms originating from marine reptiles

Filek

Lebbe

Willems

et al. 2022

Preprint

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Diatoms and bacteria are known for being the first colonizers of submerged surfaces including the skin of marine reptiles. Sea turtle carapace and skin harbour diverse prokaryotic and eukaryotic microbial taxa, including several epizoic diatoms. However, the importance of diatom-bacteria associations is hardly investigated in biofilms associated with animal hosts. This study provides a detailed inventory of diatoms, bacteria, and diatom-associated bacteria originating from several loggerhead sea turtles using a combination of metabarcoding and culturing approaches. Carapace and skin samples rbcL and 16S rRNA amplicon sequencing showed a high diversity of diatoms and bacteria, respectively. Cultures of putative epizoic and non-epizoic diatom strains contained from 18 to 101 bacterial amplicon sequence variants (ASVs) and their bacterial assemblages strongly reflected those of their source host. Diatom strains allowed for enrichment and isolation of rare-in-source bacterial families such as Marinobacteraceae, Alteromonadaceae, and Alcanivoracaceae. When accounting for phylogenetic relationships between bacterial ASVs, we observed related diatom genera might retain related microbial taxa in culture, regardless of the source environment. These data provide deeper insights into several levels of sea turtle epizoic diatom and bacterial communities, and reveal the potential of epizoic biofilms as a source of novel microbes and possibly important diatom-bacteria associations.

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“…A diverse pool of strains may be stochastically sorted into a single foundress queen’s gut, with the established population resistant to subsequent invasion [i.e., priority effects (2)]. This process may be analogous to the neutral bottlenecking described for bacterial strain partioning among skin pores (88) or the stochastic colonization of individual guts of flies and nematodes (13, 14, 19).…”

Section: Discussionmentioning

confidence: 99%

Microbiome assembly and maintenance across the lifespan of bumble bee workers

Hammer

Easton‐Calabria

Moran

2022

Preprint

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How a host’s microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for humans and a handful of other hosts, an important next step is to compare microbiome dynamics across a broader array of host-microbe symbioses, and to investigate how and why they vary. Here we characterize the temporal dynamics and stability of the bumblebee worker gut microbiome. Bumblebees are a useful symbiosis model given their relatively well-understood life history and simple, host-specific gut bacterial communities. Furthermore, microbial dynamics may influence bumblebee health and pollination services. We combined high-temporal-resolution sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics to characterize gut microbiomes over the adult lifespan of Bombus impatiens workers. To understand how hosts may control (or lose control of) the gut microbiome as they age, we also sequenced hindgut transcriptomes. We found that, at the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. At the same time, partitioning of strain-level bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome—including expression of key immunity genes—stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumblebees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession, and for comparative analyses with other host-microbe symbioses.

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Anatomy promotes neutral coexistence of strains in the human skin microbiome

Cited by 93 publications

References 95 publications

Scale-dependent tipping points of bacterial colonization resistance

Scale-dependent tipping points of bacterial colonization resistance

More than just hitchhikers: a survey of bacterial communities associated with diatoms originating from marine reptiles

Microbiome assembly and maintenance across the lifespan of bumble bee workers

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