Abstract

Ocean warming is affecting marine benthic ecosystems through mass mortality events that involve marine invertebrates, in particular bivalves, corals, and sponges. Among these events, extensive die-offs of Ircinia fasciculata sponges have been recurrently reported in western Mediterranean. The goal of our study was to test whether the temperature-related mass sponge die-offs were associated with or preceded by an early unbalanced bacterial microbiome in the sponge tissues. We took advantage of the early detection of disease and compared the microbiomes of healthy vs. early diseased I. fasciculata tissues. Our results showed a microbiome shift in early diseased tissues. The abundance of Gammaproteobacteria and Acidobacteria increased and that of Deltaproteobacteria decreased in diseased vs. healthy tissues. The change in community composition was also noticeable at the operational taxonomic unit (OTU) level. Diseased tissues contained more bacterial sequences previously identified in injured or stressed sponges and corals than healthy tissues. Bacterial diversity increased significantly in diseased tissues, which contained a higher number of low abundance OTUs. Our results do not support the hypothesis of one particular pathogen, whether a Vibrio or any other bacteria, triggering the Northwestern Mediterranean mass mortalities of I. fasciculata. Our data rather suggest an early disruption of the bacterial microbiome balance in healthy sponges through a shift in OTU abundances, and the purported consequent decline of the sponge fitness and resistance to infections. Opportunistic bacteria could colonize the sponge tissues, taking benefit of the sponge weakness, before one or more virulent pathogens might proliferate ending in the mass sponge die-off.

Highlights

  • Ocean warming is affecting marine benthic ecosystems through epidemiologic diseases and mass mortalities of invertebrates, in particular bivalves, corals and sponges (Harvell et al, 2002)

  • Fasciculata revealed an alteration of the sponge bacterial community during the first phase of a Mediterranean massive sponge die-off caused by anomalous high temperatures (Cebrian et al, 2011)

  • We hypothesize that the temperature-produced stress, to which the sponges were subjected, unbalanced the symbiotic bacterial community of healthy sponges causing changes in the sponge bacterial community composition and diversity

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Summary

Introduction

Ocean warming is affecting marine benthic ecosystems through epidemiologic diseases and mass mortalities of invertebrates, in particular bivalves, corals and sponges (Harvell et al, 2002). The mass mortality events are increasing across all oceans (Webster, 2007) and may lead to declines, or rises of other benthic species, with unpredictable subsequent effects (Pinnegar et al, 2000). In corals, where diseases have long been studied (e.g., Rosenberg and Ben-Haim, 2002; Sutherland et al, 2004), the growing theory is that diseases are caused by opportunistic polymicrobial infections, rather than by a single primary pathogen (Lesser et al, 2007; Bourne et al, 2008; Rosenberg et al, 2009). It has been proposed that coral diseases are caused by a change of some benign components of the associated microbial communities into pathogens (Lesser et al, 2007)

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