Forfeiting the priority effect: turnover defines biofilm community succession

Brislawn, Colin; Graham, Emily B.; Dana, Karl; Ihardt, Peter; Fansler, Sarah; Chrisler, William B.; Cliff, John; Stegen, James C.; Moran, James J.; Bernstein, Hans C.

doi:10.1038/s41396-019-0396-x

Cited by 95 publications

(73 citation statements)

References 56 publications

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“…Our results indicated that the differential action of ecological processes may promote different biogeographic patterns in prokaryotic and picoeukaryotic assemblages in the upper global-ocean. This is consistent with other works using similar approaches to ours indicating that protistan and bacterial assemblages are shaped by different ecological processes [39,[43][44][45]. In particular, selection, which is known to have an important role in structuring prokaryotic communities [27,28], explained a higher proportion of community turnover in surface-ocean prokaryotes (≈ 34-27% of the turnover) than in picoeukaryotes (≈ 17-11%).…”

Section: Discussionsupporting

confidence: 92%

Disentangling the mechanisms shaping the surface ocean microbiota

et al. 2020

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Background: The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S-and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. Results: We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts.

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Section: Discussionsupporting

confidence: 92%

Disentangling the mechanisms shaping the surface ocean microbiota

et al. 2020

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show abstract

“…Our results indicated that the differential action of ecological processes may promote different biogeographic patterns in prokaryotic and picoeukaryotic assemblages in the upper global-ocean. This is consistent with other works using similar approaches to ours indicating that protistan and bacterial assemblages are shaped by different ecological processes [37,[41][42][43]. In particular, selection, which is known to have an important role in structuring prokaryotic communities [25,26], explained a higher proportion of community turnover in surface-ocean prokaryotes (~34-27% of the turnover) than in picoeukaryotes (~17-11%).…”

Section: Discussionsupporting

confidence: 92%

Disentangling the mechanisms shaping the surface ocean microbiota

Logares

Deutschmann

Junger

et al. 2019

Preprint

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Background The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have largescale consequences. Yet, the underlaying ecological mechanisms structuring it are unclear. Here we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore the previous, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. Results We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts. Conclusions The differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear.

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“…Prior to oviposition, eggs are coated in a diverse consortium of microbes as they pass through the hen reproductive tract as well as the distal digestive tract (cloaca) [24]. Microbial succession within complex biofilms suggests that founder microbial species play an important role by modifying the local environment in a way that mediates filtering of further microbial inputs later in the successional process [25]. The maternal microbiota deposited on the eggshell could be a potential source of important founder species, setting the stage for a healthy GIT microbiota.…”

Section: Introductionmentioning

confidence: 99%

Eggshell and environmental bacteria contribute to the intestinal microbiota of growing chickens

Maki

Bobeck

Sylte

et al. 2020

J Animal Sci Biotechnol

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Background: The initial intestinal microbiota acquired from different sources has profound impacts on animal health and productivity. In modern poultry production practices, the source(s) of the establishing microbes and their overall contribution during development of gastrointestinal tract communities are still unclear. Using fertilized eggs from two independent sources, we assessed the impact of eggshell-and environmental-associated microbial communities on the successional processes and bacterial community structure throughout the intestinal tract of chickens for up to 6 weeks post-hatch. Results: Culturing and sequencing techniques identified a viable, highly diverse population of anaerobic bacteria on the eggshell. The jejunal, ileal, and cecal microbial communities for the egg-only, environment-only, and conventionally raised birds generally displayed similar successional patterns characterized by increasing community richness and evenness over time, with strains of Enterococcus, Romboutsia, and unclassified Lachnospiraceae abundant for all three input groups in both trials. Bacterial community structures differed significantly based on trial and microbiota input with the exception of the egg-exposed and conventional birds in the jejunum at week 1 and the ileum at week 6. Cecal community structures were different based on trial and microbiota input source, and cecal short-chain fatty acid profiles at week 6 highlighted functional differences as well. Conclusion: We identified distinct intestinal microbial communities and differing cecal short-chain fatty acid profiles between birds exposed to the microbiota associated with either the eggshell or environment, and those of conventionally hatched birds. Our data suggest the eggshell plays an appreciable role in the development of the chicken intestinal microbiota, especially in the jejunum and ileum where the community structure of the eggshellonly birds was similar to the structure of conventionally hatched birds. Our data identify a complex interplay between the eggshell and environmental microbiota during establishment and succession within the chicken gut. Further studies should explore the ability of eggshell-and environment-derived microbes to shape the dynamics of succession and how these communities can be targeted through interventions to promote gut health and mitigate food-borne pathogen colonization in poultry.

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Forfeiting the priority effect: turnover defines biofilm community succession

Cited by 95 publications

References 56 publications

Disentangling the mechanisms shaping the surface ocean microbiota

Disentangling the mechanisms shaping the surface ocean microbiota

Disentangling the mechanisms shaping the surface ocean microbiota

Eggshell and environmental bacteria contribute to the intestinal microbiota of growing chickens

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