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Differential Specificity Between Closely Related Corals and Abundant Endozoicomonas Endosymbionts Across Global Scales

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Differential Specificity Between Closely Related Corals and Abundant Endozoicomonas Endosymbionts Across Global Scales The ISME Journal (2017) 11, 186–200 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 OPEN www.nature.com/ismej ORIGINAL ARTICLE Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales Matthew J Neave1,2, Rita Rachmawati3, Liping Xun2, Craig T Michell1, David G Bourne4, Amy Apprill2 and Christian R Voolstra1 1Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia; 2Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA; 3Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA and 4Australian Institute of Marine Science and College of Science and Engineering, James Cook University Townsville, Townsville, Queensland, Australia Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridiza- tion (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning. The ISME Journal (2017) 11, 186–200; doi:10.1038/ismej.2016.95; published online 8 July 2016 Introduction symbiotic algae of the genus Symbiodinium, viruses, bacteria, archaea and fungi. This complex consor- Coral reefs are declining globally at unsustainable tium is referred to as the coral holobiont (Rohwer rates (Descombes et al., 2015), driven by stressors et al., 2002; Knowlton and Rohwer, 2003). The best- including increasing sea surface temperatures, over- ’ studied members of the coral holobiont are the coral fishing and anthropogenic inputs (De ath et al., animal host and the Symbiodinium algae, which 2012). Devising strategies for mitigating future reef provide most of the host’s energy requirements loss is challenging because corals are ‘metaorgan- ’ through photosynthates. In return, the symbiotic isms , comprised not only of the host itself, but also algae receive a safe refuge, consistent sunlight and nutrients (Goodson et al., 2001). Although coral-prokaryotic associations have been Correspondence: A Apprill, Marine Chemistry and Geochemistry recognized since the late 1970s (Ducklow and Department, Woods Hole Oceanographic Institution, Woods Hole, Mitchell, 1979; Williams et al., 1987), recent MA 02543, USA. E-mail: [email protected] advancements in sequencing technology have or CR Voolstra, Red Sea Research Center, Division of Biological revealed that microbes associated with corals are and Environmental Science and Engineering, King Abdullah distinct from those in the seawater and are diverse, University of Science and Technology (KAUST), Thuwal 23955- totaling several hundred species (Rohwer et al., 6900, Saudi Arabia. E-mail: [email protected] 2001; Kellogg, 2004; Wegley et al., 2004; Sunagawa Received 9 January 2016; revised 19 April 2016; accepted et al., 2009; Roder et al., 2013, 2014; Bayer et al., 7 June 2016; published online 8 July 2016 2013b; Pantos et al., 2015). The high diversity of Differential coral–Endozoicomonas specificity MJ Neave et al 187 these microorganisms, with many belonging advances our understanding of coral holobiont to uncultured genera, makes untangling the compli- acquisition and functioning. cated interactions between microbes, the coral host and the algal dinoflagellate partners challenging. However, certain microbial species in the coral Materials and methods holobiont can fix nitrogen (Lesser et al., 2004; Lema et al., 2014), metabolize sulfur (Raina et al., Site description and sampling 2009), provide antibiotic compounds (Reshef et al., A total of 28 reefs were sampled in seven major 2006; Ritchie, 2006) and probably have roles in geographical regions across the global range of the various other biogeochemical cycles (Kimes et al., corals S. pistillata and P. verrucosa (Figure 1; 2010). Moreover, particular microbes appear to be Supplementary Table 1). A map of the sample sites ‘ ’ ‘core’ symbionts of the holobiont, always associating was created in python using the package basemap , withaspecificcoralhost, and likely providing and the code to recreate the map is available important functional benefits to the coral holobiont at https://github.com/neavemj/microbiomeMap. At (Rohwer et al., 2001; Speck and Donachie, 2012; Jessen each reef, replicate colonies of each coral species et al., 2013; Rodriguez-Lanetty et al.,2013;Bayeret al., were sampled (if present) using snorkel or SCUBA at 2013b; Ainsworth et al., 2015). depths between 2 and 10 m. Colonies were sampled 2 One of the potential ‘core’ symbionts of many by removing ~ 5 cm fragments using a hammer and corals are the Endozoicomonas, members of the chisel, which were then placed into Whirl-Pak bags Gammaproteobacteria’s Oceanospirillaceae family (Nasco, Salida, CA, USA) underwater. At the surface, (Morrow et al., 2012; Speck and Donachie, 2012; one fragment designated for DNA extraction was Apprill et al., 2013; Jessen et al., 2013; Rodriguez- wrapped in aluminum foil and immediately frozen Lanetty et al., 2013; Bayer et al., 2013b; Lesser and in liquid nitrogen, except for the Indonesian sam- Jarett, 2014; Morrow et al., 2014; Pantos et al., 2015). ples, which were preserved in 95% ethanol. These bacteria also frequently associate with other A second coral fragment was placed into a vial of marine organisms, including gorgonians (Correa 4% paraformaldehyde for microscopy analysis. Back et al., 2013; La Rivière et al., 2013; Vezzulli et al., at the laboratory, the DNA samples were frozen to 2013; Bayer et al., 2013a; Ransome et al., 2014), − 80 °C and the paraformaldehyde samples were ascidians (Dishaw et al., 2014), tube worms (Forget stored at 4 °C. and Juniper, 2013), mollusks (Jensen et al., 2010; At all of the reefs except those in Indonesia, the Hyun et al., 2014) and fish (Mendoza et al., 2013). physiochemical properties of the seawater were Although the sequence-based evidence for Endozoi- investigated. Temperature, salinity, dissolved oxy- comonas as a core microbiome member of certain gen and pH were measured using a YSI EXO1 Multi- corals is compelling, most studies have used corals Parameter Water Quality Sonde (Yellow Springs, from only one geographic location and often meth- OH, USA), except at the Red Sea sites, which were ods across studies are not standardized, making measured using a WTW Multi 3500i multimeter comparative analyses difficult. A comprehensive (Weilheim, Germany). In addition, seawater sur- study of global reefs, with fine-scale attention to rounding the reefs was sampled for inorganic − Endozoicomonas genotypes, is required to under- nutrients (250 ml, frozen to 20 °C) and planktonic stand worldwide patterns of association between cell counts (1 ml, fixed with 4% paraformaldehyde Endozoicomonas symbionts and corals. and frozen in liquid nitrogen) and analyzed Here, we examine the microbiomes of Stylophora as previously reported (Apprill and Rappé, 2011). pistillata and Pocillopora verrucosa across their For seawater microbial community analysis, several global distribution to better understand the bacterial liters of seawater was collected, placed on ice and archaeal community composition and governing and passed through 25 mm, 0.2 μm filters (Millipore, principles, as well as the fine-scale specificity of Billerica, MA, USA) until saturated using a peristal- their core symbionts. We predict that if microorgan- tic pump. The seawater samples and filters were isms are important to healthy coral functioning and then stored at − 80 °C until analysis. have co-evolved with corals, then coral microbiomes should be similar worldwide. Indeed, both coral species harbor Endozoicomonas as their abundant DNA extraction and host phylogeny symbiont, which was found to reside in aggregates Coral fragments were removed from the − 80 °C within coral tissues. Furthermore, S. pistillata dis- freezer and immediately airbrushed using cold 1 × played a highly geographically structured micro- phosphate-buffered saline (PBS). DNA was extracted biome and was associated with Endozoicomonas from the airbrushed tissue and seawater filters with genotypes unique to each
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