Coral reefs are highly complex marine ecosystems that have been the focus of numerous studies examining the drivers of biodiversity and community dynamics [1]. As in other ecosystems, coral reef microorganisms are emerging as key members to maintaining reef health and resilience in the face of large-scale degradation due to climate change, human impacts and emerging diseases of corals (reviewed by [2]). This has resulted in increased efforts to characterize diseases of reef microbial communities, and to identify which organisms influence resilience and recovery (e.g. [3]). Recent studies have shown the importance of interactions between the coral microbiome and the larger reef community (e.g. between reef-building coral and benthic algae, [4]). However, relatively few studies have examined the microbiome associated with the most mobile members of the reef community, such as fishes (e.g. [5, 6]).
Fish microbial communities are known to be affected by multiple biotic and abiotic variables. There is evidence that fish-associated bacteria are organ-specific, species-specific and individual specific, thus comprising highly diverse communities [7–9]. While host factors seem to be the major drivers of fish gut bacterial diversity [10, 11], the physicochemical properties of the water exert a considerable effect on the diversity of fish skin-associated microbes (e.g. temperature and salinity, [12]). Despite the impact of the surrounding environment, the contribution of the water microbiota to the fish skin microbiota composition seems negligible, with fish mucosae being a highly selective environment (e.g. [13]). However, other external factors, such as direct transfer of microorganisms between fishes, might also play a major and still unexplored role [14–16]. Microbial transfer between interacting partners has been shown to be common in nature, shaping microbial consortia in humans and other animal groups (reviewed in [17, 18]), including fish [14]. Although social microbial transmission could ultimately increase microbiome complexity, which may reduce the abundance of opportunistic and/or pathogenic taxa, as seen in bees [19] or chimpanzees [18], social interactions may also facilitate pathogen transmission and consequently increase levels of infection and disease (reviewed by [20]).
One of the most iconic mutualistic interactions on coral reefs is the relationship between cleanerfishes and clients. Cleaners attract individuals from multiple species (clients) to their “cleaning stations”, which are usually fixed territories where they inspect the body of multiple client fishes per day to remove parasites, dead tissue and mucus [21]. Although many small fish species clean opportunistically, members of two genera are obligate or “dedicated” cleaners [22]. These include the cleaner wrasses (Labroides spp.) in the Indo-Pacific and the cleaner gobies (Elacatinus spp.) in the Caribbean region. Cleaner gobies of the genus Elacatinus reside on benthic substrate, moving only to make contact with client fishes [21, 23], which travel and interrupt other activities to visit cleaner gobies [24, 25]. Visits to cleaner goby stations can be influenced by multiple factors including location relative to territorial client fish [24–26], local fish abundance [27], structural complexity [28], and parasite activity and abundance [26, 29]. Consequently, the abundance and diversity of client fishes can vary widely among cleaning stations. Because of their frequent contact with heterospecifics, and therefore, high potential for microbial exchange, cleanerfish may serve as a useful animal model system to understand the role of social microbial transfer in ecological communities [16]. Indeed, a recent study comparing “cleaner” vs “non-cleaner” ecotypes of E. prochilos from Barbados found that bacterial diversity was significantly increased in “cleaner” ecotypes [15].
Here, we characterized the skin bacteria of the most ubiquitous Caribbean cleaner goby species, the sharknose goby Elacatinus evelynae, in several reefs within the US Virgin Islands, using 16S rRNA gene (V4 hypervariable region) amplicon sequencing. We specifically studied the relationship between gobies’ level of interaction with clients, and skin microbiota diversity and composition. We expected to find a relationship between microbial diversity and client diversity and geographical differences in the skin microbiota among reefs due to putative socio-environmental differences.