Garriet W. Smith

The etiology of white pox, a lethal disease of the Caribbean elkhorn coral, Acropora palmata

Populations of the shallow-water Caribbean elkhorn coral, Acropora palmata, are being decimated by white pox disease, with losses of living cover in the Florida Keys typically in excess of 70%. The rate of tissue loss is rapid, averaging 2.5 cm2⋅day−1, and is greatest during periods of seasonally elevated temperature. In Florida, the spread of white pox fits the contagion model, with nearest neighbors most susceptible to infection. In this report, we identify a common fecal enterobacterium, Serratia marcescens, as the causal agent of white pox. This is the first time, to our knowledge, that a bacterial species associated with the human gut has been shown to be a marine invertebrate pathogen.

Microbial disease and the coral holobiont.

Tropical coral reefs harbour a reservoir of enormous biodiversity that is increasingly threatened by direct human activities and indirect global climate shifts. Emerging coral diseases are one serious threat implicated in extensive reef deterioration through disruption of the integrity of the coral holobiont - a complex symbiosis between the coral animal, endobiotic alga and an array of microorganisms. In this article, we review our current understanding of the role of microorganisms in coral health and disease, and highlight the pressing interdisciplinary research priorities required to elucidate the mechanisms of disease. We advocate an approach that applies knowledge gained from experiences in human and veterinary medicine, integrated into multidisciplinary studies that investigate the interactions between host, agent and environment of a given coral disease. These approaches include robust and precise disease diagnosis, standardised ecological methods and application of rapidly developing DNA, RNA and protein technologies, alongside established histological, microbial ecology and ecological expertise. Such approaches will allow a better understanding of the causes of coral mortality and coral reef declines and help assess potential management options to mitigate their effects in the longer term.

Cause of sea fan death in the West Indies

A fungus from the genus Aspergillus is the probable agent of epizootic infections that have caused mass mortality of sea fan corals (Gorgonia ventalina) over the past 15 years,. Here we show that four strains of the fungus involved in these infections are members of the species Aspergillus sydowii, a common saprobe (an organism that lives on decaying matter) that is found in both terrestrial and marine environments. Isolates of A. sydowii taken from diseased sea fans caused new infections of sea fans in inoculation experiments, whereas isolates taken from elsewhere did not.

African and Asian Dust: From Desert Soils to Coral Reefs

Abstract Many hypotheses have been proposed to explain the decline of coral reefs throughout the world, but none adequately accounts for the lack of recovery of reefs or the wide geographical distribution of coral diseases. The processes driving the decline remain elusive. Hundreds of millions of tons of dust transported annually from Africa and Asia to the Americas may be adversely affecting coral reefs and other downwind ecosystems. Viable microorganisms, macro- and micronutrients, trace metals, and an array of organic contaminants carried in the dust air masses and deposited in the oceans and on land may play important roles in the complex changes occurring on coral reefs worldwide.

Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals

In the Caribbean, the fungus Aspergillus sydowii is currently causing an epizootic among sea fan corals (Gorgonia spp.). To elucidate potential factors that may have facilitated the emergence of this disease, we characterized and compared temperature requirements, susceptibility to coral crude extracts, and metabolic profiles of pathogenic (marine) and non-pathogenic (terrestrial) strains of A. sydowii. Growth of all A. sydowii strains were observed at all temperatures tested (22–36 °C) with an optimum of approximately 30 °C. Sea fan crude extracts inhibited growth of A. sydowii but were less effective at higher temperatures. Thus, temperature is likely to have a strong influence on the dynamics of the Gorgonia–Aspergillus interaction by promoting the growth of the pathogen while reducing the efficacy of host resistance. Metabolically, marine A. sydowii strains pathogenic to sea fans were distinct from non-pathogenic terrestrial strains.

Relationship of Vibrio Species Infection and Elevated Temperatures to Yellow Blotch/Band Disease in Caribbean Corals

ABSTRACT The bacterial and temperature factors leading to yellow blotch/band disease (YBD), which affects the major reef-building Caribbean corals Montastrea spp., have been investigated. Groups of bacteria isolated from affected corals and inoculated onto healthy corals caused disease signs similar to those of YBD. The 16S rRNA genes from these bacteria were sequenced and found to correspond to four Vibrio spp. Elevating the water temperature notably increased the rate of spread of YBD on inoculated corals and induced greater coral mortality. YBD-infected corals held at elevated water temperatures had 50% lower zooxanthella densities, 80% lower division rates, and a 75% decrease in chlorophyll a and c2 pigments compared with controls. Histological sections indicated that the algal pyrenoid was fragmented into separate segments, along with a reconfiguration and swelling of the zooxanthellae, as well as vacuolization. YBD does not appear to produce the same physiological response formerly observed in corals undergoing temperature-related bleaching. Evidence indicates that YBD affects primarily the symbiotic algae rather than coral tissue.

Microbial Communities of Coral Surface Mucopolysaccharide Layers

Microbes associated with corals form communities that differ significantly from water mass communities. Physiological and metabolic activities occurring within these close, mutualistic relationships are very different from the surrounding environment and tend to be very specific. Coral-associated microbial communities are likely to resemble microbial mats in structure. Vertical stratification of populations, from proximal toward distal regions (with respect to the surface of the coral), results in fluxes of organic and inorganic nutrients. The presence of an actively metabolizing microbiota has significant influences on overall population structure. Theoretical and observed consequences of environmental changes lead to the disruption of the ‘normal’ communities associated with healthy corals. Because it is likely that the normal microbiota protects the coral animal from invading microbes, changes in the community structure may result in the development of disease.

Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbestinum (Octocorallia, Gorgonacea)

High sea surface temperature associated with the recent El Niño was responsible for widespread coral bleaching and mortality around the globe in 1998. In addition to mortality caused by temperature and bleaching associated stresses, some of the coral mortality could be due to the outbreak of diseases among already weakened hosts. One possible example of this is the October 1998 epizootic affecting Briareum asbestinum in the Florida Keys, USA. At Carysfort, Sand Key and Western Dry Rocks, between 75 and 90% of B. asbestinum colonies were bleached with prevalence of necroses on bleached colonies ranging from 18 to 70%. Between October 1998 and January 1999, 18 to 91% of colonies on seven 25 × 2 m transects died (mean=68%). In addition, at Carysfort Reef, 65% of necrotic colonies that were tagged in October 1998 were dead by January of the following year. A grafting experiment revealed that lesion-causing infections were transmissible: lesions occurred on 50% of recipient colonies treated with diseased grafts whereas none of the grafts with healthy tissue resulted in disease. Preliminary work to isolate a causative agent yielded a cyanobacterium Scytonema sp., although work to confirm its role in the mass mortality is still on-going. By January 1999, when surviving colonies had regained their color and many lesions had healed, the cause of the Briareum asbestinum mass mortality or even whether a mass mortality had occurred, would have been difficult to ascertain. By any measure, this was a significant epizootic that would have gone undetected or been attributed to bleaching stress in the absence of our evaluation of the role of an infectious disease.

Immune defenses of healthy, bleached and diseased Montastraea faveolata during a natural bleaching event.

One prominent hypothesis regarding climate change and scleractinian corals is that thermal stress compromises immune competence. To test this hypothesis we tracked how the immune defenses of bleached, apparently healthy and yellow band disease (YBD) diseased Montastraea faveolata colonies varied with natural thermal stress in southwestern Puerto Rico. Colonies were monitored for 21 mo from the peak of the bleaching event in October 2005 to August 2007. Since sea surface temperature was significantly higher in summer and fall 2005 than 2006, year of collection was used as a proxy for temperature stress, and colony fragments collected in 2005 were compared with those collected in 2006. Mortality rate was high (43% overall) and all colonies (except one) either died or became infected with YBD by August 2007. YBD-infected tissue did not bleach (i.e. expel zooxanthellae) during the 2005 bleaching event, even when healthy tissue of these colonies bleached. Immune activity was assayed by measuring prophenoloxidase (PPO), peroxidase (POX), lysozyme-like (LYS) and antibacterial (AB) activity. Immune activity was variable between all coral samples, but there was a significant elevation of PPO activity in bleached colonies collected in 2005 relative to apparently healthy and YBD-diseased corals in 2006. In YBD-diseased colonies, LYS and AB activity were elevated in both healthy and infected tissue, indicating a systemic response; activity levels in these colonies were higher compared to those that appeared healthy. In both these immune parameters, there was a trend for suppression of activity in corals that were bleached in 2005. These data, while complicated by between-genet variability, illustrate the complex interaction between disease and temperature stress on immune function.

Yellow band and dark spot syndromes in Caribbean corals: distribution, rate of spread, cytology, and effects on abundance and division rate of zooxanthellae

Yellow band and dark spot syndromes have been frequently observed to affect coral species throughout the Caribbean within the last 10 years. These syndromes significantly impair at least three important reef-building species. Yellow band (also known as yellow blotch) appears as rings or blotches on Montastrea annularis throughout the Caribbean. The coral tissue necrosis occurs at a rate of approximately 0.6 cm/month. Transect measurements at various locations indicated that as many as 90% of M. annularis were affected by yellow band during 1997–98. Tissue samples reveal a 41–96.9% decrease in zooxanthellae/sample compared to healthy specimens, depending on distance from healthy tissue. Mitotic indices (MI) of zooxanthellae (symbiotic algae appearing as doublets) for M. annularis are 2.5%. MI in yellow band samples directly bordering healthy tissue are less than 0.9%, and zooxanthellae directly within the band bordering exposed skeleton had a mitotic index of 0.0%. This indicates impairment of zooxanthellae cell division in yellow band specimens. Zooxanthellae are not expelled and appear vacuolated and devoid of organelles. Dark spot, characterized by tissue necrosis as well as a depression of the colony surface, affects Stephanocoenia michelinii and Siderastrea siderea throughout the Caribbean. Transects showed that as many as 56% of S. michelinii and S. siderea showed signs of dark spot during 1997–98. Affected tissues of S. siderea died at a rate of 4.0 cm/month. In dark spot samples from S. siderea, the total number of zooxanthellae was 56% of that in healthy tissue; dark spot-affected specimens of S. michelinii showed a 14% decrease in the number of zooxanthellae compared to healthy tissue samples. Mitotic indices of zooxanthellae from healthy specimens of S. sidereawere 1.20% compared to 0.40% in dark spot samples. Mitotic indices of healthy S. michelinii were 1.54% compared to 0.23% in dark spot samples, also indicating a decrease in algal cell division. Zooxanthellae from dark spot tissue are swollen and darker in pigment. Due to the changes that are evident in the symbiotic algae, we suggest that both syndromes act primarily on the zooxanthellae symbiont, and secondarily on the cnidarian host.