Abstract

Mass mortality events of benthic invertebrates in the Mediterranean Sea are becoming an increasing concern with catastrophic effects on the coastal marine environment. Sea surface temperature anomalies leading to physiological stress, starvation and microbial infections were identified as major factors triggering animal mortality. However the highest occurrence of mortality episodes in particular geographic areas and occasionally in low temperature deep environments suggest that other factors play a role as well. We conducted a comparative analysis of bacterial communities associated with the purple gorgonian Paramuricea clavata, one of the most affected species, collected at different geographic locations and depth, showing contrasting levels of anthropogenic disturbance and health status. Using massive parallel 16SrDNA gene pyrosequencing we showed that the bacterial community associated with healthy P. clavata in pristine locations was dominated by a single genus Endozoicomonas within the order Oceanospirillales which represented ∼90% of the overall bacterial community. P. clavata samples collected in human impacted areas and during disease events had higher bacterial diversity and abundance of disease-related bacteria, such as vibrios, than samples collected in pristine locations whilst showed a reduced dominance of Endozoicomonas spp. In contrast, bacterial symbionts exhibited remarkable stability in P. clavata collected both at euphotic and mesophotic depths in pristine locations suggesting that fluctuations in environmental parameters such as temperature have limited effect in structuring the bacterial holobiont. Interestingly the coral pathogen Vibrio coralliilyticus was not found on diseased corals collected during a deep mortality episode suggesting that neither temperature anomalies nor recognized microbial pathogens are solely sufficient to explain for the events. Overall our data suggest that anthropogenic influence may play a significant role in determining the coral health status by affecting the composition of the associated microbial community. Environmental stressful events and microbial infections may thus be superimposed to compromise immunity and trigger mortality outbreaks.

Highlights

  • Mass mortality events of benthic invertebrates from different phyla occurred in recent years in the temperate Mediterranean Sea with catastrophic effects on the coastal marine ecosystem [1], [2]

  • Species richness of the bacterial communities associated with P. clavata was highest in coral samples collected from populations subjected to anthropogenic disturbance and disease events such as those of Po30IH, Pa63ID, and Ta30ID samples, whilst declined to less than half in corals collected from pristine populations (Fig. 3)

  • The bacterial diversity associated with P. clavata estimated by the Shannon diversity index from the operational taxonomic units (OTUs) data was high for human impacted samples varying from 2.2 to 5.0 with an average of 3.2 (SD = 1.6)

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Summary

Introduction

Mass mortality events of benthic invertebrates from different phyla (sponges, cnidarians, molluscs, ascidians, bryozoans) occurred in recent years in the temperate Mediterranean Sea with catastrophic effects on the coastal marine ecosystem [1], [2]. In addition nonresident thermodependant bacterial pathogens may take advantage both from high temperature and compromised host conditions contributing significantly to coral disease and mortality [6], [7]. We recently reported that Vibrio-TAV24 strain, belonging to the species Vibrio coralliilyticus, is involved in mass mortality events of the purple gorgonian P. clavata in the NW Mediterranean Sea [7]. Symbiotic bacteria are considered an important component of the ‘‘coral’s immune system’’ by preventing the colonization of nonresident, possibly pathogenic, bacteria [9]. Studies conducted on tropical corals have shown that, under stressful conditions, resident microbes critical to the healthy functioning of PLOS ONE | www.plosone.org

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