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.
Project description: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.
Project description:Coastal pollution and algal cover are increasing on many coral reefs, resulting in higher dissolved organic carbon (DOC) concentrations. High DOC concentrations strongly affect microbial activity in reef waters and select for copiotrophic, often potentially virulent microbial populations. High DOC concentrations on coral reefs are also hypothesized to be a determinant for switching microbial lifestyles from commensal to pathogenic, thereby contributing to coral reef degradation, but evidence is missing. In this study, we conducted ex situ incubations to assess gene expression of planktonic microbial populations under elevated concentrations of naturally abundant monosaccharides (glucose, galactose, mannose, and xylose) in algal exudates and sewage inflows. We assembled 27 near-complete (>70%) microbial genomes through metagenomic sequencing and determined associated expression patterns through metatranscriptomic sequencing. Differential gene expression analysis revealed a shift in the central carbohydrate metabolism and the induction of metalloproteases, siderophores, and toxins in Alteromonas, Erythrobacter, Oceanicola, and Alcanivorax populations. Sugar-specific induction of virulence factors suggests a mechanistic link for the switch from a commensal to a pathogenic lifestyle, particularly relevant during increased algal cover and human-derived pollution on coral reefs. Although an explicit test remains to be performed, our data support the hypothesis that increased availability of specific sugars changes net microbial community activity in ways that increase the emergence and abundance of opportunistic pathogens, potentially contributing to coral reef degradation.
Project description:The microbialization of coral reefs predicts that microbial oxygen consumption will cause reef deoxygenation. Here we tested this hypothesis by analyzing reef microbial and primary producer oxygen metabolisms. Metagenomic data and in vitro incubations of bacteria with primary producer exudates showed that fleshy algae stimulate incomplete carbon oxidation metabolisms in heterotrophic bacteria. These metabolisms lead to increased cell sizes and abundances, resulting in bacteria consuming 10 times more oxygen than in coral incubations. Experiments probing the dissolved and gaseous oxygen with primary producers and bacteria together indicated the loss of oxygen through ebullition caused by heterogenous nucleation on algae surfaces. A model incorporating experimental production and loss rates predicted that microbes and ebullition can cause the loss of up to 67% of gross benthic oxygen production. This study indicates that microbial respiration and ebullition are increasingly relevant to reef deoxygenation as reefs become dominated by fleshy algae.
Project description:Increasing dissolved inorganic carbon (DIC) concentrations associated with ocean acidification can affect marine calcifiers, but local factors, such as high dissolved organic carbon (DOC) concentrations through sewage and algal blooms, may interact with this global factor. For calcifying green algae of the genus Halimeda, a key tropical carbonate producer that often occurs in coral reefs, no studies on these interactions have been reported. These data are however urgently needed to understand future carbonate production. Thus, we investigated the independent and combined effects of DIC (pCO2 402 ?atm/ pHtot 8.0 and 996 ?atm/ pHtot 7.7) and DOC (added as glucose in 0 and 294 ?mol L-1) on growth, calcification and photosynthesis of H. macroloba and H. opuntia from the Great Barrier Reef in an incubation experiment over 16 days. High DIC concentrations significantly reduced dark calcification of H. opuntia by 130 % and led to net dissolution, but did not affect H. macroloba. High DOC concentrations significantly reduced daily oxygen production of H. opuntia and H. macroloba by 78 % and 43 %, respectively, and significantly reduced dark calcification of H. opuntia by 70%. Combined high DIC and DOC did not show any interactive effects for both algae, but revealed additive effects for H. opuntia where the combination of both factors reduced dark calcification by 162 % compared to controls. Such species-specific differences in treatment responses indicate H. opuntia is more susceptible to a combination of high DIC and DOC than H. macroloba. From an ecological perspective, results further suggest a reduction of primary production for Halimeda-dominated benthic reef communities under high DOC concentrations and additional decreases of carbonate accretion under elevated DIC concentrations, where H. opuntia dominates the benthic community. This may reduce biogenic carbonate sedimentation rates and hence the buffering capacity against further ocean acidification.
Project description:On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs.
Project description:In Tayrona National Natural Park (Colombian Caribbean), abiotic factors such as light intensity, water temperature, and nutrient availability are subjected to high temporal variability due to seasonal coastal upwelling. These factors are the major drivers controlling coral reef primary production as one of the key ecosystem services. This offers the opportunity to assess the effects of abiotic factors on reef productivity. We therefore quantified primary net (Pn ) and gross production (Pg ) of the dominant local primary producers (scleractinian corals, macroalgae, algal turfs, crustose coralline algae, and microphytobenthos) at a water current/wave-exposed and-sheltered site in an exemplary bay of Tayrona National Natural Park. A series of short-term incubations was conducted to quantify O2 fluxes of the different primary producers during non-upwelling and the upwelling event 2011/2012, and generalized linear models were used to analyze group-specific O2 production, their contribution to benthic O2 fluxes, and total daily benthic O2 production. At the organism level, scleractinian corals showed highest Pn and Pg rates during non-upwelling (16 and 19 mmol O2 m(-2) specimen area h(-1)), and corals and algal turfs dominated the primary production during upwelling (12 and 19 mmol O2 m(-2) specimen area h(-1), respectively). At the ecosystem level, corals contributed most to total Pn and Pg during non-upwelling, while during upwelling, corals contributed most to Pn and Pg only at the exposed site and macroalgae at the sheltered site, respectively. Despite the significant spatial and temporal differences in individual productivity of the investigated groups and their different contribution to reef productivity, differences for daily ecosystem productivity were only present for Pg at exposed with higher O2 fluxes during non-upwelling compared to upwelling. Our findings therefore indicate that total benthic primary productivity of local autotrophic reef communities is relatively stable despite the pronounced fluctuations of environmental key parameters. This may result in higher resilience against anthropogenic disturbances and climate change and Tayrona National Natural Park should therefore be considered as a conservation priority area.
Project description: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 ?mol l(-1) DOC and 5.5 × 10(8) cells l(-1) offshore and 68 ?mol l(-1) DOC and 3.1 × 10(8) cells l(-1) 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.
Project description:Photosynthates released by benthic primary producers (BPP), such as reef algae and scleractinian corals, fuel the dissolved organic carbon (DOC) production on tropical coral reefs. DOC concentrations near BPP have repeatedly been observed to be elevated compared to those in the surrounding water column. As the DOC release of BPP increases with increasing light availability, elevated DOC concentrations near them will, in part, also depend on light availability. Consequently, DOC concentrations are likely to be higher on the shallow, well-lit reef terrace than in deeper sections on the fore reef slope. We measured <i>in situ</i> DOC concentrations and light intensity in close proximity to the reef alga <i>Dictyota</i> sp. and the scleractinian coral <i>Orbicella faveolata</i> along a depth-dependent light gradient from 5 to 20 m depth and compared these to background concentrations in the water column. At 10 m (intermediate light), DOC concentrations near <i>Dictyota</i> sp. were elevated by 15 µmol C L<sup>-1</sup> compared to background concentrations in the water column, but not at 5 and 20 m (high and low light, respectively), or near <i>O. faveolata</i> at any of the tested depths. DOC concentrations did not differ between depths and thereby light environments for any of the tested water types. However, water type and depth appear to jointly affect <i>in situ</i> DOC concentrations across the tested depth-dependent light gradient. Corroborative <i>ex situ</i> measurements of excitation pressure on photosystem II suggest that photoinhibition in <i>Dictyota</i> sp. is likely to occur at light intensities that are commonly present on Curaçaoan coral reefs under high light levels at 5 m depth during midday. Photoinhibition may have thereby reduced the DOC release of <i>Dictyota</i> sp. and DOC concentrations in its close proximity. Our results indicate that the occurrence of elevated DOC concentrations did not follow a natural light gradient across depth. Instead, a combination of multiple factors, such as water type, light availability (including the restriction by photoinhibition), and water movement are proposed to interactively determine the DOC concentrations in the close vicinity of BPP.
Project description:Turf algae increasingly dominate benthic communities on coral reefs. Given their abundance and high dissolved organic carbon (DOC) release rates, turf algae are considered important contributors to the DOC pool on modern reefs. The release of photosynthetically fixed carbon as DOC generally, but not always, increases with increased light availability. Nutrient availability was proposed as an additional factor to explain these conflicting observations. To address this proposed but untested hypothesis, we documented the interactive contributions of light and nutrient availability on the release of DOC by turf algae. DOC release rates and oxygen production were quantified in incubation experiments at two light levels (full and reduced light) and two nutrient treatments (natural seawater and enriched seawater). In natural seawater, DOC release at full light was four times higher than at reduced light. When nutrients were added, DOC release rates at both light levels were similar to the natural seawater treatment at full light. Our results therefore show that low light in combination with low nutrient availability reduces the release of DOC by turf algae and that light and nutrient availability interactively determine DOC release rates by this important component of Caribbean reef communities.
Project description:BACKGROUND:Sponges are important suspension-feeding members of reef communities, with the collective capacity to overturn the entire water column on shallow Caribbean reefs every day. The sponge-loop hypothesis suggests that sponges take up dissolved organic carbon (DOC) and, via assimilation and shedding of cells, return carbon to the reef ecosystem as particulate organic carbon (POC). Sponges host complex microbial communities within their tissues that may play a role in carbon and nutrient cycling within the sponge holobiont. To investigate this relationship, we paired microbial community characterization (16S rRNA analysis, Illumina Mi-Seq platform) with carbon (DOC, POC) and nutrient (PO4, NOx, NH4) flux data (specific filtration rate) for 10 common Caribbean sponge species at two distant sites (Florida Keys vs. Belize, ~?1203?km apart). RESULTS:Distance-based linear modeling revealed weak relationships overall between symbiont structure and carbon and nutrient flux, suggesting that the observed differences in POC, DOC, PO4, and NOx flux among sponges are not caused by variations in the composition of symbiont communities. In contrast, significant correlations between symbiont structure and NH4 flux occurred consistently across the dataset. Further, several individual symbiont taxa (OTUs) exhibited relative abundances that correlated with NH4 flux, including one OTU affiliated with the ammonia-oxidizing genus Cenarchaeum. CONCLUSIONS:Combined, these results indicate that microbiome structure is uncoupled from sponge carbon cycling and does not explain variation in DOC uptake among Caribbean coral reef sponges. Accordingly, differential DOC assimilation by sponge cells or stable microbiome components may ultimately drive carbon flux in the sponge holobiont.