David M. Baker

Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades

Many reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. There is increasing evidence of functional significance to Symbiodinium diversity, which affects the coral holobiont’s response to changing environmental conditions. For example, corals hosting Symbiodinium from the clade D taxon exhibit greater resistance to heat-induced coral bleaching than conspecifics hosting the more common clade C. Yet, the relatively low prevalence of clade D suggests that this trait is not advantageous in non-stressful environments. Thus, clade D may only be able to out-compete other Symbiodinium types within the host habitat when conditions are chronically stressful. Previous studies have observed enhanced photosynthesis and fitness by clade C holobionts at non-stressful temperatures, relative to clade D. Yet, carbon-centered metrics cannot account for enhanced growth rates and patterns of symbiont succession to other genetic types when nitrogen often limits reef productivity. To investigate the metabolic costs of hosting thermally tolerant symbionts, we examined the assimilation and translocation of inorganic 15N and 13C in the coral Acropora tenuis experimentally infected with either clade C (sub-type C1) or D Symbiodinium at 28 and 30 °C. We show that at 28 °C, C1 holobionts acquired 22% more 15N than clade D. However, at 30 °C, C1 symbionts acquired equivalent nitrogen and 16% less carbon than D. We hypothesize that C1 competitively excludes clade D in hospite via enhanced nitrogen acquisition and thus dominates coral populations despite warming oceans.

Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance?

By forming symbiotic interactions with microbes, many animals and plants gain access to the products of novel metabolic pathways. We investigated the transfer of symbiont-derived carbon and nitrogen to the sponges Aplysina cauliformis, Aplysina fulva, Chondrilla caribensis, Neopetrosia subtriangularis and Xestospongia bocatorensis, all of which host abundant microbial populations, and Niphates erecta, which hosts a sparse symbiont community. We incubated sponges in light and dark bottles containing seawater spiked with 13C- and 15N-enriched inorganic compounds and then measured 13C and 15N enrichment in the microbial (nutrient assimilation) and sponge (nutrient transfer) fractions. Surprisingly, although most sponges hosting abundant microbial communities were more enriched in 13C than N. erecta, only N. subtriangularis was more enriched in 15N than N. erecta. Although photosymbiont abundance varied substantially across species, 13C and 15N enrichment was not significantly correlated with photosymbiont abundance. Enrichment was significantly correlated with the ratio of gross productivity to respiration (P:R), which varied across host species and symbiont phylotype. Because irradiance impacts P:R ratios, we also incubated A. cauliformis in 13C-enriched seawater under different irradiances to determine whether symbiont carbon fixation and transfer are dependent on irradiance. Carbon fixation and transfer to the sponge host occurred in all treatments, but was greatest at higher irradiances and was significantly correlated with P:R ratios. Taken together, these results demonstrate that nutrient transfer from microbial symbionts to host sponges is influenced more by host–symbiont identities and P:R ratios than by symbiont abundance.

Nitrogen biogeochemistry in the Caribbean sponge, Xestospongia muta: a source or sink of dissolved inorganic nitrogen?

Background Sponges have long been known to be ecologically important members of the benthic fauna on coral reefs. Recently, it has been shown that sponges are also important contributors to the nitrogen biogeochemistry of coral reefs. The studies that have been done show that most sponges are net sources of dissolved inorganic nitrogen (DIN; NH4 + and NO3 −) and that nitrification, mediated by their symbiotic prokaryotes, is the primary process involved in supplying DIN to adjacent reefs. Methodology/Principal Findings A natural experiment was conducted with the Caribbean sponge Xestospongia muta from three different locations (Florida Keys, USA; Lee Stocking Island, Bahamas and Little Cayman, Cayman Islands). The DIN fluxes of sponges were studied using nutrient analysis, stable isotope ratios, and isotope tracer experiments. Results showed that the fluxes of DIN were variable between locations and that X. muta can be either a source or sink of DIN. Stable isotope values of sponge and symbiotic bacterial fractions indicate that the prokaryotic community is capable of taking up both NH4 + and NO3 − while the differences in δ 15N between the sponge and bacterial fractions from the NH4 + tracer experiment suggest that there is translocation of labeled N from the symbiotic bacteria to the host. Conclusions/Significance Nitrogen cycling in X. muta appears to be more complex than previous studies have shown and our results suggest that anaerobic processes such as denitrification or anammox occur in these sponges in addition to aerobic nitrification. Furthermore, the metabolism of this sponge and its prokaryotic symbionts may have a significant impact on the nitrogen biogeochemistry on Caribbean coral reefs by releasing large amounts of DIN, including higher NH4 + concentrations that previously reported.

Link between sewage-derived nitrogen pollution and coral disease severity in Guam

The goals of this study were to evaluate the contribution of sewage-derived N to reef flat communities in Guam and to assess the impact of N inputs on coral disease. We used stable isotope analysis of macroalgae and a soft coral, sampled bimonthly, as a proxy for N dynamics, and surveyed Porites spp., a dominant coral taxon on Guams reefs, for white syndrome disease severity. Results showed a strong influence of sewage-derived N in nearshore waters, with δ(15)N values varying as a function of species sampled, site, and sampling date. Increases in sewage-derived N correlated significantly with increases in the severity of disease among Porites spp., with δ(15)N values accounting for more than 48% of the variation in changes in disease severity. The anticipated military realignment and related population increase in Guam are expected to lead to increased white syndrome infections and other coral diseases.

Isotopic and microbial indicators of sewage pollution from Stone Town, Zanzibar, Tanzania

In Stone Town, Zanzibar, sewage treatment is minimal, with a biological oxygen demand reduction to 60% and no removal of bacteria or nutrients. Here, Stone Towns sewage pollution was studied by measuring Enterococci and NH(4)(+) concentrations in seawater and δ(15)N of benthic organisms; samples were collected along the Stone Town shoreline and from offshore coral reefs. Public perceptions of sewage pollution were investigated via interviews. Enterococci from the Stone Town shoreline exceeded USEPA guidelines for recreational use. Benthic organisms from two of the four reefs were relatively enriched (δ(15)N>10 ‰), indicative of sewage derived N. δ(15)N values of organisms from Stone Town exceeded 16 ‰. A strong correlation was found between Enterococci and δ(15)N across sites, while step-wise regression indicated rainfall and tidal stage as important predictors for bacterial concentrations. These data provide an important impact assessment from which the efficacy of future policy and management change can be assessed.

Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses.

Many cnidarians host endosymbiotic dinoflagellates from the genus Symbiodinium. It is generally assumed that the symbiosis is mutualistic, where the host benefits from symbiont photosynthesis while providing protection and photosynthetic substrates. Diverse assemblages of symbiotic gorgonian octocorals can be found in hard bottom communities throughout the Caribbean. While current research has focused on the phylo- and population genetics of gorgonian symbiont types and their photo-physiology, relatively less work has focused on biogeochemical benefits conferred to the host and how these benefits vary across host species. Here we examine this symbiosis among 11 gorgonian species collected in Bocas del Toro, Panama. By coupling light and dark bottle incubations (P/R) with 13C-bicarbonate tracers, we quantified the link between holobiont oxygen metabolism with carbon assimilation and translocation from symbiont to host. Our data show that P/R varied among species, and was correlated with colony morphology and polyp size. Sea fans and sea plumes were net autotrophs (P/R>1.5), while nine species of sea rods were net heterotrophs with most below compensation (P/R<1.0). 13C assimilation corroborated the P/R results, and maximum δ13Chost values were strongly correlated with polyp size, indicating higher productivity by colonies with high polyp SA:V. A survey of gorgonian-Symbiodinium associations revealed that productive species maintain specialized, obligate symbioses and are more resistant to coral bleaching, whereas generalist and facultative associations are common among sea rods that have higher bleaching sensitivities. Overall, productivity and polyp size had strong phylogenetic signals with carbon fixation and polyp size showing evidence of trait covariance.

Metabolic diversity and niche structure in sponges from the Miskito Cays, Honduras

Hosting symbionts provides many eukaryotes with access to the products of microbial metabolism that are crucial for host performance. On tropical coral reefs, many (High Microbial Abundance [HMA]) but not all (Low Microbial Abundance [LMA]) marine sponges host abundant symbiont communities. Although recent research has revealed substantial variation in these sponge-microbe associations (termed holobionts), little is known about the ecological implications of this diversity. We investigated the expansion of diverse sponge species across isotopic niche space by calculating niche size (as standard ellipse area [SEAc]) and assessing the relative placement of common sponge species in bivariate (δ13C and δ15N) plots. Sponges for this study were collected from the relatively isolated reefs within the Miskito Cays of Honduras. These reefs support diverse communities of HMA and LMA species that together span a gradient of photosymbiont abundance, as revealed by chlorophyll a analysis. HMA sponges occupied unique niche space compared to LMA species, but the placement of some HMA sponges was driven by photosymbiont abundance. In addition, photosymbiont abundance explained a significant portion of the variation in isotope values, suggesting that access to autotrophic metabolism provided by photosymbionts is an important predictor in the location of species within isotopic space. Host identity accounted for over 70% of the variation in isotope values within the Miskito Cays and there was substantial variation in the placement of individual species within isotopic niche space, suggesting that holobiont metabolic diversity may allow taxonomically diverse sponge species to utilize unique sources of nutrients within a reef system. This study provides initial evidence that microbial symbionts allow sponges to expand into novel physiochemical niche space. This expansion may reduce competitive interactions within coral reefs and promote diversification of these communities.

Variations in nitrate isotope composition of wastewater effluents by treatment type in Hong Kong

Stable isotopes (δ(15)N, δ(18)O) can serve as tracers for sources of nitrogen in the receiving environment. Hong Kong discharges ~3×10(6)m(3)d(-1) of treated wastewater into the ocean from 68 facilities implementing preliminary to tertiary treatment. We sampled treated sewage from 18 plants across 5 treatment types and examined receiving seawater from northeast Hong Kong. We analyzed nitrate and nitrite (NO3(-)+NO2(-), hereafter NOx) ammonium (NH4(+)), phosphate (PO4(+)) concentrations and δ(15)NNOx, δ(18)ONOx. Sewage effluents contained high mean nutrient concentrations (NO3(-)=260μmolL(-1), NH4(+)=1400μmolL(-1), PO4(+)=50μmolL(-1)) with some indication of nitrogen removal in advanced treatment types. Mean δ(15)NNOx of sewage effluents from all plants and treatment types (12‰) was higher than natural sources and varied spatially and seasonally. There was no overall effect of sewage treatment type on δ(15)NNOx. A mass balance model indicated that sewage (>68%) remains a dominant source of nitrate pollution in seawater in Tolo Harbor.

To swim or not to swim? A disagreement between microbial indicators on beach water quality assessment in Hong Kong.

The USEPA and the WHO now advocate the use of enterococci as indicators for marine water quality. This study investigated the outcomes for Hong Kong beach water quality assessment by comparing enterococcus measures with data from the HKEPDs monitoring programme. Six beaches were tested once every 2-3 months from November 2013 to June 2014 in order to identify the most contaminated sites, followed by intensive water sampling in sites found to have the highest enterococci densities (Clear Water Bay Second and Golden) every five to six days for six sampling events over a 30-day period in 2014. The geometric means of enterococci were found to be 124 and 41 cfu/100 mL at Clear Water Bay Second and Golden respectively, indicating that there may be higher risks of illness associated with swimming at both beaches than previously known. Moreover, beach sediments contained higher concentrations of enterococci than water, and warrant further study.

Upside-down but headed in the right direction: Review of the highly versatile Cassiopea xamachana system

The upside-down jellyfish Cassiopea xamachana (Scyphozoa: Rhizostomeae) has been predominantly studied to understand its interaction with the endosymbiotic dinoflagellate algae Symbiodinium. As an easily culturable and tractable cnidarian model, it is an attractive alternative to stony corals to understanding the mechanisms driving establishment and maintenance of symbiosis. Cassiopea is also unique in requiring the symbiont in order to complete its transition to the adult stage, thereby providing an excellent model to understand symbiosis-driven development and evolution. Recently, the Cassiopea research system has gained interest beyond symbiosis in fields related to embryology, climate ecology, behavior, and more. With these developments, resources including genomes, transcriptomes, and laboratory protocols are steadily increasing. This review provides an overview of the broad range of interdisciplinary research that has utilized the Cassiopea model and highlights the advantages of using the model for future research. We dedicate this manuscript to Robert Trench, who inspired many of us to begin working in Cassiopea