Abstract

Contemporary in-depth sequencing of environmental samples has provided novel insights into microbial community structures, revealing that their diversity had been previously underestimated. Communities in marine environments are commonly composed of a few dominant taxa and a high number of taxonomically diverse, low-abundance organisms. However, studying the roles and genomic information of these “rare” organisms remains challenging, because little is known about their ecological niches and the environmental conditions to which they respond. Given the current threat to coral reef ecosystems, we investigated the potential of corals to provide highly specialized habitats for bacterial taxa including those that are rarely detected or absent in surrounding reef waters. The analysis of more than 350,000 small subunit ribosomal RNA (16S rRNA) sequence tags and almost 2,000 nearly full-length 16S rRNA gene sequences revealed that rare seawater biosphere members are highly abundant or even dominant in diverse Caribbean corals. Closely related corals (in the same genus/family) harbored similar bacterial communities. At higher taxonomic levels, however, the similarities of these communities did not correlate with the phylogenetic relationships among corals, opening novel questions about the evolutionary stability of coral-microbial associations. Large proportions of OTUs (28.7–49.1%) were unique to the coral species of origin. Analysis of the most dominant ribotypes suggests that many uncovered bacterial taxa exist in coral habitats and await future exploration. Our results indicate that coral species, and by extension other animal hosts, act as specialized habitats of otherwise rare microbes in marine ecosystems. Here, deep sequencing provided insights into coral microbiota at an unparalleled resolution and revealed that corals harbor many bacterial taxa previously not known. Given that two of the coral species investigated are listed as threatened under the U.S. Endangered Species Act, our results add an important microbial diversity-based perspective to the significance of conserving coral reefs.

Highlights

  • Microorganisms dominate the oceans’ total biomass [1], phylogenetic diversity and metabolic activity

  • Ranking of the unique V6-tags sampled from reef water by abundance yielded a low number of dominant taxa, results similar to those previously reported for other marine environments [3,5,21]

  • We identified more than 20,000 V6-tags that were unique to coral samples (Figure 1B)

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Summary

Introduction

Microorganisms dominate the oceans’ total biomass [1], phylogenetic diversity and metabolic activity. One of the most remarkable findings has been that diverse microbial taxa exist at very low abundances while accounting for much of the total diversity in various marine environments [3]. This ‘‘rare biosphere’’ stands largely unexplored, but is inherently linked to several important questions [5]. It is unknown whether low-abundance microbes are restricted to particular environments or universally dispersed [6]. Rare organisms may become abundant, if not dominant, in response to environmental or habitat changes, i.e., when conditions shift to become more suitable for rapid growth. The identification of environmental conditions and/or ecological habitats specialized to support rare and underexplored bacteria are critical steps toward a better understanding of the evolutionary mechanisms and ecological forces that drive the biogeography, population structure, and temporal dynamics of the marine microbial biosphere

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