Variability of Symbiodinium Communities in Waters, Sediments, and Corals of Thermally Distinct Reef Pools in American Samoa

RESEARCH ARTICLE Variability of Symbiodinium Communities in Waters, Sediments, and Corals of Thermally Distinct Reef Pools in American Samoa Ross Cunning1*, Denise M. Yost1, Marisa L. Guarinello2, Hollie M. Putnam1, Ruth D. Gates1 1 University of Hawai‘i, Hawai‘i Institute of Marine Biology, PO Box 1346, Kāne‘ohe, Hawaii, 96744, United States of America, 2 Northwest Knowledge Network, University of Idaho, 875 Perimeter Dr. MS2358, Moscow, Idaho, 83844, United States of America * Abstract OPEN ACCESS Citation: Cunning R, Yost DM, Guarinello ML, Putnam HM, Gates RD (2015) Variability of Symbiodinium Communities in Waters, Sediments, and Corals of Thermally Distinct Reef Pools in American Samoa. PLoS ONE 10(12): e0145099. doi:10.1371/journal.pone.0145099 Editor: Chaolun Allen Chen, Biodiversity Research Center, Academia Sinica, TAIWAN Received: July 31, 2015 Accepted: November 28, 2015 Published: December 29, 2015 Copyright: © 2015 Cunning et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All data and analysis scripts are available at Dryad (doi:10.5061/dryad. 32md8). Funding: This work was funded by the National Park Service in a collaboration between RDG and the National Park of American Samoa. Additional funding was provided by the United States Geological Survey to RDG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Reef-building corals host assemblages of symbiotic algae (Symbiodinium spp.) whose diversity and abundance may fluctuate under different conditions, potentially facilitating acclimatization to environmental change. The composition of free-living Symbiodinium in reef waters and sediments may also be environmentally labile and may influence symbiotic assemblages by mediating supply and dispersal. The magnitude and spatial scales of environmental influence over Symbiodinium composition in different reef habitat compartments are, however, not well understood. We used pyrosequencing to compare Symbiodinium in sediments, water, and ten coral species between two backreef pools in American Samoa with contrasting thermal environments. We found distinct compartmental assemblages of clades A, C, D, F, and/or G Symbiodinium types, with strong differences between pools in water, sediments, and two coral species. In the pool with higher and more variable temperatures, abundance of various clade A and C types differed compared to the other pool, while abundance of D types was lower in sediments but higher in water and in Pavona venosa, revealing an altered habitat distribution and potential linkages among compartments. The lack of between-pool effects in other coral species was due to either low overall variability (in the case of Porites) or high within-pool variability. Symbiodinium communities in water and sediment also showed within-pool structure, indicating that environmental influences may operate over multiple, small spatial scales. This work suggests that Symbiodinium composition is highly labile in reef waters, sediments, and some corals, but the underlying drivers and functional consequences of this plasticity require further testing with high spatial resolution biological and environmental sampling. Introduction Coral reefs are among the most biologically diverse ecosystems on Earth and provide valuable ecosystem services as sources of tourism, coastal protection, natural products, primary PLOS ONE | DOI:10.1371/journal.pone.0145099 December 29, 2015 1 / 17 Symbiodinium Community Variability Competing Interests: The authors have declared that no competing interests exist. productivity, and nutrition [1]. At the foundation of these ecosystems is the symbiosis between corals and diverse unicellular dinoflagellates in the genus Symbiodinium, which provide corals the nutrition they need to build calcium carbonate skeletons and accrete large reef structures [2]. Reefs are declining worldwide in large part due to the breakdown of this symbiosis (coral “bleaching” [3]) in response to environmental stressors, particularly high sea surface temperature anomalies, which are predicted to become more frequent and severe with climate change [4]. However, plasticity in corals’ symbiotic associations, i.e., their ability to associate with different Symbiodinium partners that are better adapted to different environmental conditions, may allow corals to acclimatize as conditions change [5,6]. Indeed, different Symbiodinium partners may alter the growth, energetics, and heat tolerance of their coral hosts [7,8]. Whether dynamic symbioses may realistically benefit corals under rapid climate change is unclear [9], in part due to a poor understanding of the ecological drivers of Symbiodinium community assembly and stability on reefs. The composition of coral symbiont assemblages is influenced by both innate symbiotic specificity or flexibility [10,11] and environmental conditions at multiple spatial scales [12,13]. Contrasting patterns of stability or change in the dominant (i.e., most numerically abundant) symbiont type of different coral species across environmental gradients suggest that symbioses may be flexible in some corals but not others [14]. However, in addition to dominant symbionts, diverse lower-abundance taxa may also be present and dynamic, although they have been historically understudied due to methodological constraints [11,15]. More comprehensive and quantitative studies leveraging next-generation sequencing (NGS) are now emerging [16–20] and are necessary to understand how whole Symbiodinium assemblages are structured and influenced by the environment. Symbiont community composition may also be influenced by Symbiodinium present in nearby hosts as well as in other reef habitat compartments, such as sediments and seawater. These free-living Symbiodinium communities generally are distinct from, but overlap with, endosymbiotic diversity [21–23], but have not yet been fully characterized by NGS. Linkages between free-living and symbiotic communities are expected, as Symbiodinium are routinely expelled by symbiotic hosts [24], actively dispersed by host larvae and corallivorous fishes [25– 27], and exogenously acquired by both juvenile [28,29] and adult [30] hosts. Therefore, a metacommunity framework, in which an array of local communities are connected by dispersal [31], may provide insight into the drivers and scales of Symbiodinium community assembly on reefs [32]. In this context, it is also critical to understand how free-living communities in other reef habitat compartments are structured and influenced by the environment, which until now has received little study [23]. Here, we investigate environmental influence on Symbiodinium communities in reef wa (...truncated)