Vibrio infections triggering mass mortality events in a warming Mediterranean Sea

Abstract

Mass mortality events of benthic invertebrates in the temperate north-western (NW) Mediterranean Sea have been observed in recent seasons. A 16 month in situ study in the Ligurian Sea (NW Mediterranean Sea) demonstrated that the occurrence of Paramuricea clavata mortality episodes were concomitant to a condition of prolonged high sea surface temperatures, low chlorophyll concentrations and the presence of culturable Vibrio spp. in seawater. The occurrence of Vibrio spp. at the seasonal scale was correlated with temperature; with few vibrios retrieved on specific media when the temperature dropped below 18 degrees C and a sharp increase of vibrios abundance (up to 3.4 x 10(4) MPN l(-1)) when the temperature was greater than or equal to 22 degrees C. Phylogenetic and phenotypic analysis of Vibrio isolates associated with healthy and diseased P. clavata colonies collected during a mortality episode showed that these bacteria were significantly more abundant in diseased than in healthy corals and were related to the V. harveyi, V. splendidus and V. coralliilyticus groups, the latter only identified in diseased organisms. Inoculation of bacterial isolates from these groups onto healthy P. clavata in aquaria caused disease signs and death in a range of Vibrio concentrations, temperature values and trophic conditions consistent with those recorded in the field. It is concluded that Vibrio infections may act as an additional triggering mechanism of mass mortality events in the coastal Mediterranean Sea and that their occurrence is climate-linked. Predicted global warming leading to long-lasting hot summer periods together with stratification resulting in energetic constraints represent a major threat to the survival of benthic invertebrates in the temperate NW Mediterranean Sea due to potential disease outbreak associated with Vibrio pathogens.

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

“…High summer temperatures correlate with increased V. cholerae outbreaks (Fernandez et al, 2009;Hashizume et al, 2011), as well as infections caused by V. parahaemolyticus and V. vulnificus (Iwamoto et al, 2010). Increased SST undoubtedly causes an increase in abundance of vibrios (Vezzulli et al, 2010); however, temperature also has a more direct role in Vibrio pathogenicity (Oh et al, 2009), although little is known regarding specific mechanisms involved in temperature-related infections.…”

“…Although it is uncertain whether V. coralliilyticus is a primary or opportunistic coral pathogen, evidence strongly suggests that this endemic member of global coral holobionts (Pollock et al, 2010) has a role in coral disease (Rosenberg and Kushmaro, 2011). Infection experiments establish the ability of V. coralliilyticus to cause bacterial bleaching (Ben-Haim et al, 2003b), white syndrome (Sussman et al, 2008) and mortality in corals (Alves et al, 2010;Vezzulli et al, 2010), in addition to being associated with the microbial consortium of black band disease (Arotsker et al, 2009). V. coralliilyticus type strain ATCC (American Type Culture Collection, Manassas, VA, USA) BAA-450 (Vc450), isolated from bleached corals near Zanzibar, displays a tightly regulated temperature-dependent virulence; it is capable of invading and lysing coral tissue of Pocillopora damicornis at temperatures 427 1C, it attacks the symbiotic algae of this coral at temperatures between 24 1C and 26.5 1C and is avirulent at temperatures p24 1C (Ben-Haim et al, 2003b).…”

“…Pathogens of the genus Vibrio are associated with temperature-related diseases exhibiting peak infection rates in humans (Igbinosa and Okoh, 2008) and corals (Vezzulli et al, 2010) following the warmer summer months. High summer temperatures correlate with increased V. cholerae outbreaks (Fernandez et al, 2009;Hashizume et al, 2011), as well as infections caused by V. parahaemolyticus and V. vulnificus (Iwamoto et al, 2010).…”

“…In addition, we use two-dimensional liquid chromatography coupled with tandem mass spectrometry and bioassays to investigate the influence of nonpathogenic (24 1C) and pathogenic (27 1C) temperatures on the expression of virulence Figure 1 Global distribution of V. coralliilyticus strains. The V. coralliilyticus strains represented here are (a) type strains (Ben-Haim et al, 2003a), as well as strains identified using (b) DnaJ PCR (Vezzulli et al, 2010), (c, d) 16S rRNA sequencing (Sussman et al, 2008;Kesarcodi-Watson et al, 2009), (e) multi-locus sequencing (Alves et al, 2010) and (f) multiple molecular analyzes, that is, 16S rRNA sequencing, recA PCR and repetitive extragenic palindromic -polymerase chain reaction (REP-PCR) (Vizcaino et al, 2010).…”

“…coralliilyticus is of interest because of its global distribution, broad host range and temperaturedependent pathogenicity in corals. V. coralliilyticus has been isolated from marine organisms in the Atlantic (Ben-Haim et al, 2003a;Alves et al, 2010;Vizcaino et al, 2010), Indian (Ben-Haim et al, 2003a) and Pacific Oceans (Sussman et al, 2008;Kesarcodi-Watson et al, 2009), as well as the Mediterranean (Vezzulli et al, 2010) and Red Seas (Ben-Haim et al, 2003a) (Figure 1). It causes fatal infections in a wide range of organisms, including unicellular algae (Ben-Haim et al, 2003b;de Oliveira Santos et al, 2011), corals (Ben-Haim et al, 2003b), oysters (Jeffries, 1982), shrimp (Austin et al, 2005;de Oliveira Santos et al, 2011), rainbow trout (Austin et al, 2005) and flies (Alves et al, 2010;de Oliveira Santos et al, 2011) during experimental infection assays.…”