Effects of Coral Reef Benthic Primary Producers on Dissolved Organic Carbon and Microbial Activity

Abstract

Benthic primary producers in marine ecosystems may significantly alter biogeochemical cycling and microbial processes in their surrounding environment. To examine these interactions, we studied dissolved organic matter release by dominant benthic taxa and subsequent microbial remineralization in the lagoonal reefs of Moorea, French Polynesia. Rates of photosynthesis, respiration, and dissolved organic carbon (DOC) release were assessed for several common benthic reef organisms from the backreef habitat. We assessed microbial community response to dissolved exudates of each benthic producer by measuring bacterioplankton growth, respiration, and DOC drawdown in two-day dark dilution culture incubations. Experiments were conducted for six benthic producers: three species of macroalgae (each representing a different algal phylum: Turbinaria ornata – Ochrophyta; Amansia rhodantha – Rhodophyta; Halimeda opuntia – Chlorophyta), a mixed assemblage of turf algae, a species of crustose coralline algae (Hydrolithon reinboldii) and a dominant hermatypic coral (Porites lobata). Our results show that all five types of algae, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. In general, primary producers with the highest rates of photosynthesis released the most DOC and yielded the greatest bacterioplankton growth; turf algae produced nearly twice as much DOC per unit surface area than the other benthic producers (14.0±2.8 µmol h−1 dm−2), stimulating rapid bacterioplankton growth (0.044±0.002 log10 cells h−1) and concomitant oxygen drawdown (0.16±0.05 µmol L−1 h−1 dm−2). Our results demonstrate that benthic reef algae can release a significant fraction of their photosynthetically-fixed carbon as DOC, these release rates vary by species, and this DOC is available to and consumed by reef associated microbes. These data provide compelling evidence that benthic primary producers differentially influence reef microbial dynamics and biogeochemical parameters (i.e., DOC and oxygen availability, bacterial abundance and metabolism) in coral reef communities.

Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages

“…Special care was taken to exclude specimens infested with epibionts or endolithic boring organisms to avoid potential contamination of the targeted exudates. Further details on sample collection can be found in a companion paper (Haas et al, 2011).…”

“…Differences in the amount and composition of labile dissolved organic carbon (DOC) exuded by corals and algae as a portion of their daily production may support this feedback by influencing the growth rate and community composition of bacterioplankton in the surrounding water (Smith et al, 2006;Haas et al, 2011;Kelly et al, 2012). These DOC exudates may have a central role in coral-algal interactions and reef biogeochemical processes, but little is known of the composition of these exudates or the bacterial communities for which they may select.…”

“…One of the primary resources for heterotrophic marine microorganisms is dissolved organic matter (DOM), a heterogenous pool of compounds that varies widely in composition and lability (Hansell and Carlson, 2002). The bulk of the accumulated DOM in surface waters of the tropical oceans is resistant to rapid microbial degradation on the timescales of weeks to months (Carlson, 2002), but in shallow nearshore habitats, various benthic organisms have been shown to release significant quantities of DOM, of which a portion is more bioavailable than the bulk background DOM pool (Ducklow, 1990;Haas et al, 2011). Alteration of the metabolism or composition of microbial communities through release of bioavailable DOM has been hypothesized as an indirect mechanism by which algae may facilitate coral decline, possibly through microbialinduced hypoxic stress (Smith et al, 2006) or through selection of opportunistically pathogenic microorganisms (Dinsdale and Rohwer, 2011).…”

“…These results indicate that reef DOM supports a unique community able to metabolize both reef-derived and oceanic DOM, but experimental tests of these processes are required to clarify these relationships. Seawater culture techniques, in which a naturally occurring population of bacteria is inoculated in particle-free seawater media, allows for the simultaneous monitoring of bacterioplankton growth and DOM utilization and is one approach used to assess the availability of DOM to natural assemblages of bacterioplankton Carlson and Ducklow, 1996;Haas et al, 2011). By analyzing shifts in community structure among dilution cultures amended with DOM of varying composition, changes in community structure can be coupled with cell growth and DOM utilization to infer linkages between structure and function (Carlson et al, 2004;Carlson, 2011, 2012).…”

Energetic differences between bacterioplankton trophic groups and coral reef resistance

“…DDAM predicts that stressors such as overfishing and eutrophication release turf and fleshy macroalgae from grazing control, leading to increased release rates of labile DOC. DOC stimulates heterotrophic microbial growth [18][19][20][21], some of which are opportunistic coral pathogens [22]. These pathogens kill corals and create more space for the algae.…”