Local Conditions Influence the Prokaryotic Communities Associated With the Mesophotic Black Coral Antipathella subpinnata

Abstract

Black corals are important habitat-forming species in the mesophotic and deep-sea zones of the world’s oceans because of their arborescent colony structure and tendency to form animal forests. Although we have started unraveling the ecology of mesophotic black corals, the importance of the associated microbes to their health has remained unexplored. Here, we provide in-depth assessments of black coral-microbe symbioses by investigating the spatial and temporal stability of these associations, and make comparisons with a sympatric octocoral with similar colony structure. To this end, we collected samples of Antipathella subpinnata colonies from three mesophotic shoals situated along the Ligurian Coast of the Mediterranean Sea (Bordighera, Portofino, Savona) in the spring of 2017. At the Portofino shoal, samples of A. subpinnata and the gorgonian Eunicella cavolini were collected in November 2016 and May 2017. Bacterial communities were profiled using 16S rRNA gene amplicon sequencing. The bacterial community of E. cavolini was consistently dominated by Endozoicomonas . Contrastingly, the black coral microbiome was more diverse, and was primarily composed of numerous Bacteroidetes, Alpha- and Gammaproteobacterial taxa, putatively involved in all steps of the nitrogen and sulfur cycles. Compositional differences in the A. subpinnata microbiome existed between all locations and both time points, and no phylotypes were consistently associated with A. subpinnata . This highlights that local conditions may influence the bacterial community structure and potentially nutrient cycling within the A. subpinnata holobiont. But it also suggests that this coral holobiont possesses a high degree of microbiome flexibility, which may be a mechanism to acclimate to environmental change.

Thermal stress responses of the antipatharian Stichopathes sp. from the mesophotic reef of Mo'orea, French Polynesia

“…These recycling organisms are unlikely to be Symbiodiniaceae as our fragments seemed to be azooxanthellate (based on histological and metabarcoding analyses, data not shown). Several studies revealed the high diversity (Liu et al, 2018;Santiago-Vázquez et al, 2007) and plasticity (van de Water et al, 2020) in microbial communities associated with antipatharian corals, which role in nitrogen cycling within the holobiont has been demonstrated previously in scleractinians (Middelburg et al, 2016;Szmant et al, 1990;see Rädecker et al, 2015 for review). Here, microbial diversity was not investigated genetically, but histological analyses revealed the presence of cell-associated microbial aggregates (CAMAs) in the ectoderm of the tentacles (Figure 6b).…”

“…The skeleton of antipatharians is made of chitin and proteins (Goldberg, 1978;Goldberg, 1994;Juárez-de la Rosa et al, 2012;Kim et al, 1992) and is sought to be used for medical, religious or decorative purposes, or sold as precious corals in the jewellery trade in several regions across the globe (Bruckner et al, 2008;Bruckner, 2016;Grigg, 2001;Tsounis et al, 2010;Todinanahary et al, 2016). Diverse microbial communities were described within and around antipatharian tissues (Dannenberg et al, 2015;Liu et al, 2018;Penn et al, 2006;Santiago-Vázquez et al, 2007;van de Water et al, 2020;Zhang et al, 2012). They are known to play significant roles in antipatharian health, and may be a key player for acclimatization and/or adaptation to future environmental changes (Bosch & McFall-Ngai, 2011;McFall-Ngai et al, 2013;van de Water et al, 2020).…”

“…Diverse microbial communities were described within and around antipatharian tissues (Dannenberg et al, 2015;Liu et al, 2018;Penn et al, 2006;Santiago-Vázquez et al, 2007;van de Water et al, 2020;Zhang et al, 2012). They are known to play significant roles in antipatharian health, and may be a key player for acclimatization and/or adaptation to future environmental changes (Bosch & McFall-Ngai, 2011;McFall-Ngai et al, 2013;van de Water et al, 2020). While antipatharians have long been referred to as azooxanthellate species, recent studies have shown the presence of Symbiodiniaceae within the tissues of various families of antipatharians (Antipathidae, Aphanipathidae, Myriopathidae and Schizopathidae; Bo et al, 2011;Wagner et al, 2011).…”

Consensus Guidelines for Advancing Coral Holobiont Genome and Specimen Voucher Deposition

“…Many studies feature 16S rRNA gene amplicon sequencing to describe the microbiome of corals. Large datasets, such as obtained for the Earth Microbiome Project, maximize the comparability among studies (Thompson et al, 2017), but the employed primers are prone to misamplification in corals and provide limited coverage of some taxonomic groups (Bayer et al, 2013;Robbins et al, 2019;van de Water et al, 2020). Such methodological constraints may resolve in the near future with the availability of direct full-length sequencing of 16S rRNA genes (Carradec et al, 2020).…”

Black Coral Distribution in the Italian Seas: A Review

“…The different entities of fishing disturbance could also be linked to different coral morphologies. In fact, the morphological characteristics (arborescent and erect structures) and the grade of flexibility of black corals may increase their resistance to mechanical friction, showing different mechanical responses to their entanglement [24,43,65].…”