Abstract

To better understand how complex microbial communities become assembled on eukaryotic hosts, it is essential to disentangle the balance between stochastic and deterministic processes that drive their assembly. Deterministic processes can create consistent patterns of microbiome membership that result in persistent resident communities, while stochastic processes can result in random fluctuation of microbiome members that are transient with regard to their association to the host. We sampled oyster reefs from six different populations across the east coast of the United States. At each site we collected gill tissues for microbial community analysis and additionally collected and shipped live oysters to Northeastern University where they were held in a common garden experiment. We then examined the microbiome shifts in gill tissues weekly for 6 weeks using 16S rRNA gene amplicon sequencing. We found a strong population-specific signal in the microbial community composition of field-sampled oysters. Surprisingly, the oysters sampled during the common garden experiment maintained compositionally distinct gill-associated microbial communities that reflected their wild population of origin, even after rearing them in a common garden for several weeks. This indicates that oyster gill-associated microbiota are predominantly composed of resident microbes specific to host population, rather than being a reflection of their immediate biotic and abiotic surroundings. However, certain bacterial taxa tended to appear more frequently on individuals from different populations than on individuals from the same population, indicating that there is a small portion of the gill microbiome that is transient and is readily exchanged with the environmental pool of microbes. Regardless, the majority of gill-associated microbes were resident members that were specific to each oyster population, suggesting that there are strong deterministic factors that govern a large portion of the gill microbiome. A small portion of the microbial communities, however, was transient and moved among oyster populations, indicating that stochastic assembly also contributes to the oyster gill microbiome. Our results are relevant to the oyster aquaculture industry and oyster conservation efforts because resident members of the oyster microbiome may represent microbes that are important to oyster health and some of these key members vary depending on oyster population.

Highlights

  • Host-associated microbial communities play vital roles in host development, nutrition, and even behavior (McFall-Ngai et al, 2013)

  • We found that the majority of amplicon sequence variants (ASVs) in our experiment were resident to their oyster population, i.e., they were more often found among oysters within the same population than across multiple populations, even at the end of the common garden experiment

  • To disentangle the relative contributions of deterministic and stochastic processes to the microbial community assembly of adult oysters, we identified resident members and transient members of the oyster microbiome

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Summary

Introduction

Host-associated microbial communities play vital roles in host development, nutrition, and even behavior (McFall-Ngai et al, 2013). Because of their ubiquity and importance to host physiology, the field of biology has been challenged to rethink what constitutes an individual organism (Rohwer et al, 2002; Rosenberg et al, 2007; Gordon et al, 2013; Bordenstein and Theis, 2015) and how animals evolve (Rosenberg and Zilber-Rosenberg, 2013). Stochastic processes (e.g., neutral community assembly) can explain microbial community dynamics in some free-living microbial assemblages, where random immigration plays an important role in shaping microbial communities (Ofiteru et al, 2010). Most studies on microbial community assembly mechanisms suggest that both deterministic and stochastic processes play significant roles in structuring microbial communities

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