Viruses in the mucus layer of scleractinian corals

Viruses attract increasing interest from environmental microbiologists seeking to understand their function and role in coral health. Viruses can cause profound changes in the commensal prokaryotic and eukaryotic communities, which may lead to coral disfunctioning or diseases, or can conversely act as a natural phage therapy for diseased scleractinians by removing bacterial pathogen. There is a lack of basic ecological information regarding viruses, such as in situ abundance in corals, their variability among the large diversity of scleractinian species, their colonization processes and the ecological links with their hosts. In this study by Nguyen-Kim et al., (2014), the specific objectives were to determine the concentrations of coral-associated viruses in the superficial mucus layer of seven different scleractinian species collected in a coral reef of Whale Island (Vietnam), compare

their abundance with that measured in the surrounding water, and investigate the potential links between viral distribution in coral and the abundance, physiology and diversity of their bacterial hosts.

On average, the concentrations of viruses and bacteria were, respectively, 17- and two-fold higher in the mucus than in the surrounding water. The examination of bacterial community composition also showed remarkable differences between mucus and water samples. The percentage of active respiring cells was nearly threefold higher in mucus than in water. Interestingly, a positive and highly significant correlation was observed between the proportion of active cells and viral abundance in the mucus, suggesting that the metabolism of the bacterial associates is probably a strong determinant of the distribution of viruses within the coral holobiont.

Recently, high virus-to-prokaryote ratios (VPRs) have also been recorded in the mucus layer of different aquatic organisms, including corals, and this has become the foundation of a novel paradigm, called the bacteriophage-adherence-to-mucus (BAM) model. This model  demonstrates that the mucus inhabiting viruses constitutes an efficient biological barrier against bacterial pathogen colonization. According to the BAM model, the great abundance of phages in the mucus layer can be explained by the high adhesive affinities between phages and the mucinproteins of the mucus. As the result of the lytic action of such pathogens, the model predicts that bacterial abundance in mucus will be thus reduced, and conversely that of viruses will increase, unavoidably leading to an increase of the VPR. Dissolved organic matter composition has been demonstrated to shape bacterial diversity, and mucus provides a large abundance of particular substrates that select for a community composed of specialists (likely symbionts). The availability of substrates is expected to select for different functions and composition of the host communities, and therefore to also select for their specific phage communities.

In biotopes with high virus concentrations, such as in coral mucus, one might thus expect high host diversity according to the ‘kill the winner’ hypothesis. However, the absence of correlation between viral abundance and the DGGE diversity indices within the data set does not support this postulate. One of the reasons might be because DDGE method only reveals the diversity of the most dominant members of the prokaryotic community, and that most of the diversity is probably located in the rarest biosphere. Another reason would be that the bacterial community comprised few competitive specialists that account for most of the diversity. Furthermore lysogeny might also be more important than expected in coral mucus, which could explain the absence of clear links between the abundance of free viral particles and diversity indices of their host.

Coral mucus, given its unique physicochemical characteristics and sticking properties, can be regarded as a highly selective biotope for a specialized symbiotic microbial life associated with highly abundant viruses. The physiological state of the prokaryotic associates was seemingly the best determinant of viral abundance in the mucus, suggesting that most of the coral-associated viruses are phages, which might be produced by the most active fraction of the cells, through a lytic pathway. Further studies are now needed to make an accurate evaluation of lytic and lysogenic mediated infections to get better insights into the effective role of viruses in the coral microbiological balance. The results of the present study open new perspectives for the investigation of these understudied viral particles in reef environments. Temporal and spatial variability in coral communities may result in changes in relationships between viruses and bacteria so a wider range of sampling sites and dates need to be included to give a better understanding of coral microbial communities.

Nguyen‐Kim, H., Bouvier, T., Bouvier, C., Doan‐Nhu, H., Nguyen‐Ngoc, L., Rochelle‐Newall, E., ... & Bettarel, Y. (2014). High occurrence of viruses in the mucus layer of scleractinian corals. Environmental Microbiology Reports, 6(6), 675-682.

http://onlinelibrary.wiley.com/doi/10.1111/1758-2229.12185/pdf