Abstract

Examination of host-microbe interactions in early diverging metazoans, such as cnidarians, is of great interest from an evolutionary perspective to understand how host-microbial consortia have evolved. To address this problem, we analyzed whether the bacterial community associated with the cosmopolitan and model sea anemone Exaiptasia pallida shows specific patterns across worldwide populations ranging from the Caribbean Sea, and the Atlantic and Pacific oceans. By comparing sequences of the V1–V3 hypervariable regions of the bacterial 16S rRNA gene, we revealed that anemones host a complex and diverse microbial community. When examined at the phylum level, bacterial diversity and abundance associated with E. pallida are broadly conserved across geographic space with samples, containing largely Proteobacteria and Bacteroides. However, the species-level makeup within these phyla differs drastically across space suggesting a high-level core microbiome with local adaptation of the constituents. Indeed, no bacterial OTU was ubiquitously found in all anemones samples. We also revealed changes in the microbial community structure after rearing anemone specimens in captivity within a period of four months. Furthermore, the variation in bacterial community assemblages across geographical locations did not correlate with the composition of microalgal Symbiodinium symbionts. Our findings contrast with the postulation that cnidarian hosts might actively select and maintain species-specific microbial communities that could have resulted from an intimate co-evolution process. The fact that E. pallida is likely an introduced species in most sampled localities suggests that this microbial turnover is a relatively rapid process. Our findings suggest that environmental settings, not host specificity, seem to dictate bacterial community structure associated with this sea anemone. More than maintaining a specific composition of bacterial species some cnidarians associate with a wide range of bacterial species as long as they provide the same physiological benefits towards the maintenance of a healthy host. The examination of the previously uncharacterized bacterial community associated with the cnidarian sea anemone model E. pallida is the first global-scale study of its kind.

Highlights

  • Insights into the microbiome diversity of metazoan hosts have triggered a considerable interest in uncovering the regulatory principles underlying host/microbe interactions across multicellular organisms

  • The highest average bacterial Operational taxonomic units (OTU) richness were obtained from the E. pallida samples obtained from a commercial pet store (1,671 ± 144) and the CC7 clonal population samples reared in the lab (1,358 ± 225), which were approximately four and three times higher respectively than anemones with the lowest OTU richness from a natural population in Hawaii (409 ± 227)

  • This study revealed the previously uncharacterized bacterial community associated with the cnidarian sea anemone model Exaiptasia pallida at different locations throughout the Northern Hemisphere

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Summary

Introduction

Insights into the microbiome diversity of metazoan hosts have triggered a considerable interest in uncovering the regulatory principles underlying host/microbe interactions across multicellular organisms. In the case of Hydra viridis (Medusozoa: Hydrozoa), induced absence of a microbial community in host polyps causes strong developmental defects and reduces asexual reproduction via budding (Rahat & Dimentman, 1982). This suggests that the evolution of microbes and host interactions dates back to earlier diverging metazoan lineages (i.e., cnidarians), which has triggered an imperative interest to understand whether bacterial cores comprised of specific species have evolved in intimate association with their hosts since the early times of metazoan evolution (Bosch & Miller, 2016)

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