Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change

Abstract

In the temperate north-western Mediterranean Sea, large-scale disease outbreaks in benthic invertebrate species have recently occurred during climatic anomalies characterized by elevated seawater temperatures. One of the most affected species was the red gorgonian Paramuricea clavata, a key species of highly diverse communities dwelling in dim-lit habitats in the Mediterranean. From diseased P. clavata colonies, we isolated culturable bacteria associated to tissue lesions in order to investigate their potential as pathogens. Inoculation of four bacterial isolates onto healthy P. clavata in aquaria caused disease signs similar to those observed during the 2003 mortality event. The infection process was dependent on elevated seawater temperatures, in a range of values consistent with recordings performed in the field during the climatic anomalies. Among the four isolates, we identified a Vibrio coralliilyticus strain that showed virulence to P. clavata. This strain was re-isolated from diseased colonies during the experimentations. V. coralliilyticus has been previously identified as a thermodependent pathogen of a tropical coral species, emphasizing a causal role of this infectious agent in the P. clavata disease. Taking into consideration predicted global warming over the coming decades, a better understanding of the factors and mechanisms that affect the disease process will be of critical importance in predicting future threats to temperate gorgonians communities in the Mediterranean Sea.

Global warming-enhanced stratification and mass mortality events in the Mediterranean

“…According to the energetic constraints hypothesis, the loss in biomass would be the end result of a metabolic imbalance between the high energy expenditure due to respiration at high summer temperatures combined with low energy income due to low food availability in the summer. The experimental results conform to the field observations, and both the experimental and field results support the energetic constraints hypothesis, because (i) the biomass of colonies affected by a mortality event was below the threshold experimentally observed to determine the appearance of partial mortality, (ii) the variation in the timing of occurrence of partial mortality in the treatments was due to differences in the rate of biomass loss, (iii) the loss of biomass in the ambient-temperature-ambient-food treatment was similar to that observed in situ in late summer, (iv) the loss of biomass did not occur when supplemental food was provided at ambient temperatures, and (v) the alternative hypothesis related to the exposure to lethal temperature and/or to pathogenic microorganisms causes tissue cell death without biomass loss (21,22).…”

“…But although lethal temperatures should not be disregarded, they did not characterize the environmental framework of the events (17), and microorganisms present on colonies during occurrence of the events were interpreted as opportunistic (11,19; but see ref. 21). The fact that mass mortality events preferentially affect taxa that exhibit energy shortages, such as suspension-feeding gorgonians and sponges (12,20), suggests that energetic constraints due to high metabolic activity and prolonged low levels of food should be explored as a potential determinant of mass mortality events.…”

“…The occurrence of such climatic anomalies in late summer implies prolonged exposure of organisms dwelling above the thermocline to summer conditions (high temperatures and low food availability). In this framework, the main hypotheses regarding the causes of invertebrate mass mortality events are related to the exposure of benthic organisms to (i) temperatures above their level of thermal tolerance, (ii) temperatures below critical temperatures but producing physiological stress, and (iii) virulence of microorganisms (11,12,17,(19)(20)(21)(22). But although lethal temperatures should not be disregarded, they did not characterize the environmental framework of the events (17), and microorganisms present on colonies during occurrence of the events were interpreted as opportunistic (11,19; but see ref.…”

Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages

“…In particular, exudates from Turbinaria differentially selected for OTUs within the generic clades of Vibrio/Photobacterium, Pseudoalteromonas and Alteromonas (Figure 3 and Table 5), each of which composed between 3% and 5% of the total 16S reads to collectively dominate the communities (Supplementary Table S5). Each of these clades contains cultured isolates putatively associated with coral disease (Kushmaro et al, 2001;Ben-Haim et al, 2003;Costa-Ramos and Rowley, 2004;Bally and Garrabou, 2007). However, we emphasize that these VF analyses are supportive, rather than definitive evidence for the enhanced pathogenicity of algal-enriched communities.…”

Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation

“…It can be seen that eight of the nine Vibrio species (Supplementary Table S1) that have close relatives among our coral mucus cultivars have been implicated in the pathogenesis of marine organisms or humans, and seven of these vibrios were isolated from bleached corals (Ritchie et al, 1994;Thompson et al, 2005;Bourne et al, 2008), although only one, V. coralliilyticus, has been directly proven to be an etiological agent of bleaching in P. damicornis (Ben-Haim and Rosenberg, 2002). V. coralliilyticus is also a causative agent of white syndrome disease in other coral species (Bally and Garrabou, 2007;Sussman et al, 2008Sussman et al, , 2009Vezzulli et al, 2010).…”