Holobiont Diversity in a Reef-Building Coral over Its Entire Depth Range in the Mesophotic Zone

Fanny L Gonzalez-Zapata,Gretchen Walljasper,Juan A Sanchez,Catalina Ramírez-Portilla,Pim Bongaerts,Boahemaa Adu-Oppong,Alejandro Reyes

doi:10.3389/fmars.2018.00029

Abstract

Mesophotic reef-building coral communities (~30-120 m depth) remain largely unexplored, despite representing roughly three-quarters of the overall depth range at which tropical coral reef ecosystems occur. Although many coral species are restricted to shallow depths, several species occur across large depth ranges, including lower mesophotic depths. Yet, it remains unclear how such species can persist under extreme low-light conditions and how the different symbiotic partners associated with these corals contribute to facilitate such broad depth ranges. We assessed holobiont genetic diversity of the Caribbean coral Agaricia undata over depth in three localities of Colombia: San Andres Island (between 37 and 85 m), Cartagena (between 17 and 45 m) and Parque Nacional Natural Corales de Profundidad (between 77 and 87 m). We used a population genomics approach (NextRAD) for the coral host, and amplicon sequencing for the associated Symbiodinium (non-coding region of the plastid psbA minicircle) and prokaryotic (V4 region of the 16S rRNA gene) symbiont community. For the coral host, genetic structuring was only observed across geographic regions, but not between depths. Bayesian clustering and discriminant analysis of principal components revealed genetic structuring between the three regions, but not between shallow ( 60 m) depths. This pattern was confirmed when evaluating pairwise differentiation (FST) between populations, with much higher values between regions (0.0467-0.1034) compared to between depths [within location; -0.0075-(-0.0007)]. Symbiotic partners, including seven types of zooxanthellae and 325 prokaryotic OTUs, did not exhibit partitioning across depths. All samples hosted Symbiodinium clade C3 and the type C3psbA_e was present in all depths. Alpha microbial diversity was not significantly different between zones (upper vs. lower), which community composition between coral colonies was similar in the two zones (ANOSIM, R = -0.079, P > 0.05). The coral microbiome was dominated by Uncultured Betaproteobacteria in the order EC94 (16%), Unknown-Bacteria (15%), family Cenarchaeaceae (12 %), Burkholderiaceae (10%), and Hahellaceae (10%). The constant coral-holobiont composition along the studied depth range suggests that identity of the symbionts is not responsible for the coral's broad depth range and adaptation to low light environments.

Highlights

Symbiotic relationships in aquatic environments are widespread and play important roles for the health, adaptation, and evolution of the host organisms (Grossart et al, 2013)
We evaluated host genetic differentiation across populations using genome-wide single nucleotide polymorphisms (SNPs) and assessed symbiotic communities using targeted amplicon sequencing of the psbAncr for Symbiodinium and 16S ribosomal RNA gene for prokaryotes
The ecological success of this species across these depth ranges does not seem to be the result of genetic adaptation of the coral host, or due to the hosting of distinct specialized symbiont communities over depth

Summary

Introduction

Symbiotic relationships in aquatic environments are widespread and play important roles for the health, adaptation, and evolution of the host organisms (Grossart et al, 2013). The most recognized example of symbioses in marine ecosystems is the association between the coral polyps and photosynthetic algae belonging to the genus Symbiodinium (Stat et al, 2008). The importance of the coral-Symbiodinium symbiosis is exceptional, since the success of corals (the foundation species of the most biodiverse marine ecosystem) in oligotrophic tropical waters largely contribute to this symbiosis. Corals associate with prokaryotes (Bacteria and Archaea), a symbiosis that can provide important resources to the host through biogeochemical cycling of carbon, nitrogen, and sulfur (Wild et al, 2004; Raina et al, 2013; Radecker et al, 2015). The species composition of these microbiota can vary among colonies of the same host species, a fact that has been related to environmental differences (Klaus et al, 2007; Kahng et al, 2014; Ziegler et al, 2017), health status (Kimes et al, 2010) and biological traits (Bongaerts et al, 2013; Glasl et al, 2017)

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Results

Conclusion