Local dynamics of a white syndrome outbreak and changes in the microbial community associated with colonies of the scleractinian brain coral Pseudodiploria strigosa

Abstract

Reef corals in the Mexican Reef System have been severely affected by the emergence of a white syndrome that resembles both White Plague II and SCTLD descriptions. Meandroid scleractinian coral species are among the most severely affected. To gain insight into this affliction we conducted a broad study in the brain coral Pseudodiploria strigosa at a rear reef site in the NE Mexican Caribbean. We describe macro and microscopical signals of the disease, characterize the outbreak dynamics, the tissue histopathology, explore immunological responses in the individuals, and compare microbial assemblages associated with the surface mucus layer of healthy and unhealthy colonies. At the study site, the white syndrome outbreak on P. strigosa showed a high incidence rate in summer-fall and a low one in winter, as well as low survival expectation of diseased colonies at the end of the study. After 306 days of observation, out of 96 tracked colonies, eight remained apparently healthy and seven were diseased. No effective resistance to colony disease progression was observed once white syndrome signs developed. Tissue loss rate during the study varied among colonies (mean = 10.8 cm2, s.d. = 7.8 cm2) suggesting a complex relation between causal agents and colony resistance. The deterioration of tissues was evidenced from the basal to the surface body wall of polyps (up to 66% hypertrophy and liquefactive necrosis in unhealthy colonies), implying that microscopic alterations begin before macroscopic signals develop, suggesting this may be a systemic disease. We measured high levels of phenoloxidase (two orders of magnitude higher PO activity than P. strigosa affected by BBD) and antibacterial activity without significant reduction in unhealthy samples from the mucus layer, indicative of an enhanced immunological response. Results showed that opportunistic bacteria dominated damaged colonies, where six genera of the Bacteroidia class were found with significant changes in unhealthy colonies after DeSeq2 analysis. Nevertheless, histological observations did not support infection of the tissues. The opportunistic overload seems to be contained within the mucus layer but may be associated with the mortality of tissues in a yet unclear way. Future research should focus on experimental infections, the tracking of natural infections, and the immunocompetence of corals in the face of environmental pressures due to local, regional, and global impacts. If environmental deterioration is the primary cause of the continuing emergence and re-emergence of lethal coral diseases, as has been proposed by many authors, the only true option to effectively help preserve the coral reef biodiversity and services, is to restore the environmental quality of reef waters at the local scale and reduce greenhouse gases at the global scale.

Variable Species Responses to Experimental Stony Coral Tissue Loss Disease (SCTLD) Exposure

“…Therefore, this experimental design may have "leveled the playing field, " allowing for equivalent exposure among species to pathogenic material, which may not exist in nature. Histopathological analysis of a small subset of samples from the experiment found similar tissue markers of disease as previous SCTLD studies (Landsberg et al, 2020;Thome et al, 2021), suggesting similar physiological impacts once infected. Diseased samples of all six experimental species showed greater symbiont vacuolization and exocytosis than healthy samples.…”

Short- and Long-Term Effectiveness of Coral Disease Treatments

“…For example, gastrodermal necrosis was found in 87% of visually diseased histological samples as well as in 11% of apparently healthy areas of tissue (Landsberg et al, 2020). And microbial communities on apparently healthy tissue of affected colonies are sometimes similar to those of unaffected colonies while other times more similar to those at active lesions (Meyer et al, 2019;Rosales et al, 2020;Thome et al, 2021). It has also been suggested that the bacteria seen in microbiome studies are purely opportunistic, capitalizing on other underlying health issues (Landsberg et al, 2020).…”

“…3. Thome et al (2021) tagged 96 P. strigosa colonies on an SCTLD-affected reef in Mexico; within 306 days, mortality was greater than 84%, with nearly half of the surviving colonies actively diseased at that point. 4.…”

Spatial Patterns of a Lethal White Syndrome Outbreak in Pseudodiploria strigosa

“…The spreading spatial patterns have suggested a primary infectious causal agent and diminishing tissue loss rates in affected colonies treated with antibiotics reinforce the idea that a bacterial infection is involved in SCTDL syndrome development (Neely et al, 2020). Nevertheless, so far, although several putative bacterial agents have been proposed (Aeby et al, 2019;Meyer et al, 2019;Paul et al, 2019;Iwanowicz et al, 2020;Thomé et al, 2021) no causality has been demonstrated, only association, which is not evidenced enough (Hill, 1965;Evans, 1976). Moreover, given the above, it seems that opportunistic pathogens may play a confusing role to the extent that Aeby et al (2019) consider that not just bacteria, but viruses or even protozoa may play a causal role in the SCTLD.…”