The coral ecosphere: A unique coral reef habitat that fosters coral–microbial interactions

Abstract

Scleractinian corals are bathed in a sea of planktonic and particle‐associated microorganisms. The metabolic products of corals influence the growth and composition of microorganisms, but interactions between corals and seawater microorganisms are underexplored. We conducted a field‐based survey to compare the biomass, diversity, composition, and functional capacity of microorganisms in small‐volume seawater samples collected adjacent to five coral species with seawater collected > 1 m away from the reef substrate on the same reefs. Seawater collected close to corals generally harbored copiotrophic‐type bacteria and its bacterial and archaeal composition was influenced by coral species as well as the local reef environment. Trends in picoplankton abundances were variable and either increased or decreased away from coral colonies based on coral species and picoplankton functional group. Genes characteristic of surface‐attached and potentially virulent microbial lifestyles were enriched in near‐coral seawater compared to reef seawater. There was a prominent association between the coral Porites astreoides and the coral symbiont Endozoicomonas, suggesting recruitment and/or shedding of these cells into the surrounding seawater. This evidence extends our understanding of potential species‐specific and reef site‐influenced microbial interactions that occur between corals and microorganisms within this near‐coral seawater environment that we propose to call the “coral ecosphere.” Microbial interactions that occur within the coral ecosphere could influence recruitment of coral‐associated microorganisms and facilitate the transfer of coral metabolites into the microbial food web, thus fostering reef biogeochemical cycling and a linkage between corals and the water column.

Diel, daily, and spatial variation of coral reef seawater microbial communities

“…These conditions may impact microbial community composition as well as potential microbial functions in the seawater surrounding corals at the scale of the momentum boundary layer [27,32,36], a layer of water surrounding the coral that is influenced by coral morphology and micro-currents caused by animal activity within the coral [35]. In fact, there is evidence that distinct microbial environments exist within 30 cm surrounding coral colonies in an environment called the coral ecosphere [37]. For example, coral ecosphere microbial communities were generally enriched with copiotrophic Gammaproteobacteria compared to microbial communities sampled from water >1 meter above the reef [37] and this finding corroborated earlier observations of copiotrophic enrichment in the seawater adjacent to corals [32].…”

“…In fact, there is evidence that distinct microbial environments exist within 30 cm surrounding coral colonies in an environment called the coral ecosphere [37]. For example, coral ecosphere microbial communities were generally enriched with copiotrophic Gammaproteobacteria compared to microbial communities sampled from water >1 meter above the reef [37] and this finding corroborated earlier observations of copiotrophic enrichment in the seawater adjacent to corals [32]. Additionally, the Gammaproteobacteria Endozoicomonas, a ubiquitous coral tissue and mucus symbiont, was enriched within the ecosphere surrounding P. astreoides, indicating that the ecosphere environment may serve as a reservoir for coral symbionts and pathogens [37].…”

Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

“…2-4). However, symbiotic S. 'fitti' strains might be attracted to the different microbial composition and abundance in the water column adjacent to a coral colony that constitute the 'ecosphere' surrounding each acroporid (Weber, González-Díaz, Armenteros, & Apprill 2019). Similarly, the food associated with each 'ecospheres' may attract different Symbiodiniaceae (Pollock et al 2018;Weber et al 2019).…”

“…However, symbiotic S. 'fitti' strains might be attracted to the different microbial composition and abundance in the water column adjacent to a coral colony that constitute the 'ecosphere' surrounding each acroporid (Weber, González-Díaz, Armenteros, & Apprill 2019). Similarly, the food associated with each 'ecospheres' may attract different Symbiodiniaceae (Pollock et al 2018;Weber et al 2019). Putative intraspecific variation in the swimming availability and chemosensory responses of S. 'fitti' may also, in part, dictate which Symbiodiniaceae persist in each ecosphere (Fitt 1984;Fitt 1985;Fitt, Chang, & Trench 1981;Kamykowski, Reed, & Kirkpatrick 1992).…”

The potential of parrotfish faeces in replenishing reefs with coral-associated microbiome

“…The relevance of enriching reef sediments relies on coral health and resilience. Sediments enhance the coral uptake of Symbiodinaceae cells (Adams et al, 2009), which is relevant for coral recruitment and health recovery after bleaching events (Adams et al, 2009;Ali et al, 2019), and facilitate the enrichment of the coral's ecosphere with beneficial microbes and therefore, supports coral physiological responses from microbial exchange processes (Weber et al, 2019).…”