Depleted dissolved organic carbon and distinct bacterial communities in the water column of a rapid-flushing coral reef ecosystem

Abstract

Coral reefs are highly productive ecosystems bathed in unproductive, low-nutrient oceanic waters, where microbially dominated food webs are supported largely by bacterioplankton recycling of dissolved compounds. Despite evidence that benthic reef organisms efficiently scavenge particulate organic matter and inorganic nutrients from advected oceanic waters, our understanding of the role of bacterioplankton and dissolved organic matter (DOM) in the interaction between reefs and the surrounding ocean remains limited. In this study, we present the results of a 4-year study conducted in a well-characterized coral reef ecosystem (Paopao Bay, Moorea, French Polynesia) where changes in bacterioplankton abundance and dissolved organic carbon (DOC) concentrations were quantified and bacterial community structure variation was examined along spatial gradients of the reef:ocean interface. Our results illustrate that the reef is consistently depleted in concentrations of both DOC and bacterioplankton relative to offshore waters (averaging 79 lmol l À1 DOC and 5.5 Â 10 8 cells l À1 offshore and 68 lmol l À1 DOC and 3.1 Â 10 8 cells l À1 over the reef, respectively) across a 4-year time period. In addition, using a suite of culture-independent measures of bacterial community structure, we found consistent differentiation of reef bacterioplankton communities from those offshore or in a nearby embayment across all taxonomic levels. Reef habitats were enriched in Gamma-, Delta-, and Betaproteobacteria, Bacteriodetes, Actinobacteria and Firmicutes. Specific bacterial phylotypes, including members of the SAR11, SAR116, Flavobacteria, and Synechococcus clades, exhibited clear gradients in relative abundance among nearshore habitats. Our observations indicate that this reef system removes oceanic DOC and exerts selective pressures on bacterioplankton community structure on timescales approximating reef water residence times, observations which are notable both because fringing reefs do not exhibit long residence times (unlike those characteristic of atoll lagoons) and because oceanic DOC is generally recalcitrant to degradation by ambient microbial assemblages. Our findings thus have interesting implications for the role of oceanic DOM and bacterioplankton in the ecology and metabolism of reef ecosystems.

Variability in Microbial Community Composition and Function Between Different Niches Within a Coral Reef

“…However, these observations are in contrast to a previous work demonstrating significant differences in microbial community composition between sample sites on coral reefs at Lizard Island (GBR), Magnetic Island (GBR) and Tobago (Caribbean) [14,16,26]. Nelson et al [27] examined the spatio-temporal variations throughout Paopao Bay (French Polynesia) by measuring changes in the community composition between waters from the bay, the reef and the open ocean, revealing distinctly different phylogenetic features of the bacterial communities between sites. The microbial communities inhabiting healthy, diseased and bleached Acroporas from American Samoa and the Great Barrier Reef have also recently been shown to demonstrate compositional shifts under natural bleaching and disease events, with the abundance of Vibrio bacteria increasing during bleaching [28,29].…”

“…Previous research has used metagenomics to reveal large changes in microbial community composition and function between different coral reefs [18,19]. However, while 16S rRNA-based approaches have shown that microbial community composition can shift within reef systems [14,16,26,27], patterns in microbial functional potential across different niches within a single coral reef ecosystem had not previously been documented.…”

Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors

“…As a result, they included species-specific bacterial components of the coral holobiont (1), as well as specific bacterial taxa associated with some algal functional groups (1,25). In addition, the microbial communities sampled on these reefs reflected selection by the adjacent benthic macroorganisms, as evidenced by the differences between reef-associated bacterioplankton communities and open ocean communities (26). There is evidence that reef-associated communities undergo selection in shallow reef environments by the locally available labile organic matter exuded by the benthic organisms (27).…”

Biogeography of the Sediment Bacterial Community Responds to a Nitrogen Pollution Gradient in the East China Sea

“…4). Although it is widely accepted that depth is an important factor in controlling the vertical distribution of bacteria in the soil and in the water column (38,43), our emphasis in this study is on the role of depth in a landscape, rather than along a vertical column.…”