Influence of coral and algal exudates on microbially mediated reef metabolism

Abstract

Benthic primary producers in tropical reef ecosystems can alter biogeochemical cycling and microbial processes in the surrounding seawater. In order to quantify these influences, we measured rates of photosynthesis, respiration, and dissolved organic carbon (DOC) exudate release by the dominant benthic primary producers (calcifying and non-calcifying macroalgae, turf-algae and corals) on reefs of Mo‘orea French Polynesia. Subsequently, we examined planktonic and benthic microbial community response to these dissolved exudates by measuring bacterial growth rates and oxygen and DOC fluxes in dark and daylight incubation experiments. All benthic primary producers exuded significant quantities of DOC (roughly 10% of their daily fixed carbon) into the surrounding water over a diurnal cycle. The microbial community responses were dependent upon the source of the exudates and whether the inoculum of microbes included planktonic or planktonic plus benthic communities. The planktonic and benthic microbial communities in the unamended control treatments exhibited opposing influences on DO concentration where respiration dominated in treatments comprised solely of plankton and autotrophy dominated in treatments with benthic plus plankon microbial communities. Coral exudates (and associated inorganic nutrients) caused a shift towards a net autotrophic microbial metabolism by increasing the net production of oxygen by the benthic and decreasing the net consumption of oxygen by the planktonic microbial community. In contrast, the addition of algal exudates decreased the net primary production by the benthic communities and increased the net consumption of oxygen by the planktonic microbial community thereby resulting in a shift towards net heterotrophic community metabolism. When scaled up to the reef habitat, exudate-induced effects on microbial respiration did not outweigh the high oxygen production rates of benthic algae, such that reef areas dominated with benthic primary producers were always estimated to be net autotrophic. However, estimates of microbial consumption of DOC at the reef scale surpassed the DOC exudation rates suggesting net consumption of DOC at the reef-scale. In situ mesocosm experiments using custom-made benthic chambers placed over different types of benthic communities exhibited identical trends to those found in incubation experiments. Here we provide the first comprehensive dataset examining direct primary producer-induced, and indirect microbially mediated alterations of elemental cycling in both benthic and planktonic reef environments over diurnal cycles. Our results highlight the variability of the influence of different benthic primary producers on microbial metabolism in reef ecosystems and the potential implications for energy transfer to higher trophic levels during shifts from coral to algal dominance on reefs.

Year-Long Monitoring of Physico-Chemical and Biological Variables Provide a Comparative Baseline of Coral Reef Functioning in the Central Red Sea

“…Coral reef bacterial biofilms had a far higher species richness and diversity compared to Red Sea coral reef water or coral microbiomes [21,59,60,62]. Bacterial and algal biofilms were variable (29% of bacterial and 99% of algal communities significantly varied in abundance between reefs and seasons), and an increase in bacterial diversity during spring and summer coincided with significantly increased algal growth, supporting the notion of interaction between algal and bacterial communities via exudates [38,39]. Furthermore, significant variability between the warm and cool season provides insight into potential community changes associated with ocean warming.…”

“…Epilithic algal turfs and crusts comprise a great part of reef primary production and constitute an essential food source for grazing reef fish [36,37]. Epilithic algae provide substrate for bacterial growth with different algal exudates selecting for specific bacterial communities [38,39], which also impact coral recruitment. While algal turfs reduce the settlement of marine invertebrates and inhibit the survival of coral recruits [40–42], crusts of coralline algae promote and induce the settlement of coral larvae [43].…”

Sponge exhalent seawater contains a unique chemical profile of dissolved organic matter

“…For example, macroalgae generally produce exudates that are higher in neutral sugars and in DOC concentration than coral exudates (Haas et al, 2011; Nelson et al, 2013). Studies comparing DOC from different sources and their effects on ecosystem function have begun to elucidate ecologically important connections between DOC, microbial community composition, and coral reef biogeochemical cycling (e.g., Wild et al, 2008; Haas et al, 2013). …”

“…The composition of DOM can influence the population structure of microbial communities (Landa et al, 2013), including those in coral reef seawater and sediment (Haas et al, 2013; Nelson et al, 2013). DOM composition also influences coral health (Morrow et al, 2012) and ecosystem-wide nutrient cycling (Wild et al, 2004).…”

Biological oxygen demand optode analysis of coral reef-associated microbial communities exposed to algal exudates

“…However, the accompanying study by Haas et al (2013b) indicates that responses of reef-associated microbial communities are significantly more dependent on the source of exudates than concentration.…”