Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella D. Tye Pettaya,b,1, Drew C. Whama, Robin T. Smithc,d, Roberto Iglesias-Prietoc, and Todd C. LaJeunessea,e,1 aDepartment of Biology, The Pennsylvania State University, University Park, PA 16802; bCollege of Earth, Ocean, and Environment, University of Delaware, Lewes, DE 19958; cUnidad Académica de Sistemas Arrecifales (Puerto Morelos), Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, CP 77500 Cancún, Mexico; dScience Under Sail Institute for Exploration, Sarasota, FL 34230; and ePenn State Institutes of Energy and the Environment, University Park, PA 16802 Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved April 28, 2015 (received for review February 11, 2015) Human-induced environmental changes have ushered in the rapid coral communities distributed across broad geographic areas decline of coral reef ecosystems, particularly by disrupting the over the decadal ecological timescales that are necessary to keep symbioses between reef-building corals and their photosymbionts. pace with the current rate of warming. However, escalating stressful conditions enable some symbionts Research on the diversity and ecology of coral symbionts to thrive as opportunists. We present evidence that a stress-tolerant suggests that episodes of stressful warming may facilitate the “zooxanthella” from the Indo-Pacific Ocean, Symbiodinium trenchii, spread of ecologically rare or opportunistic species (13). The has rapidly spread to coral communities across the Greater Carib- severe mass bleaching and mortality of eastern Caribbean corals bean. In marked contrast to populations from the Indo-Pacific, in 2005 corresponded with an increased prevalence and abun- Atlantic populations of S. trenchii contained exceptionally low dance of Symbiodinium trenchii (formerly D1a,orD1-4) (15), a genetic diversity, including several widespread and genetically species in Clade D. This group is distantly related to other similar clones. Colonies with this symbiont tolerate temperatures lineages of Symbiodinium and is primarily known for occurring in 1–2 °C higher than other host–symbiont combinations; however, animals at the margins of their environmental tolerance (15). calcification by hosts harboring S. trenchii is reduced by nearly Before, during, and after this bleaching event, S. trenchii spread half, compared with those harboring natives, and suggests that to many coral species, especially among those ultimately showing ECOLOGY these new symbioses are maladapted. Unforeseen opportunism the greatest signs of physiological trauma (i.e., bleaching). Col- and geographical expansion by invasive mutualistic microbes onies with high densities of this symbiont seemed to tolerate could profoundly influence the response of reef coral symbioses significant thermal stress. Indeed, photosynthetic rates of to major environmental perturbations but may ultimately com- S. trenchii (in hospite) remain unaffected at temperatures that promise ecosystem stability and function. are typically stressful to other Symbiodinium spp. (16–18). When environmental conditions stabilized, however, S. trenchii was invasive species | climate change | reef corals | calcification | symbiosis inexorably displaced (requiring months or years) by host-typical symbionts (13, 19). Therefore, the persistence of S. trenchii iological invasions and global climate change are drastically within a coral colony may depend on chronic, or acute, stressors. Baltering the diversity, distribution, and ecology of all biota on We suspected, for several reasons, that S. trenchii populations the planet (1–4), which negatively affects human well-being (5). in the northwestern tropical Atlantic (i.e., Greater Caribbean) Although the body of literature on invasive plants and animals is voluminous, invasions by nonpathogenic microbes and their Significance impacts on ecosystem functions are poorly documented (6). Microbial invasions are difficult to detect, especially among free- This research documents the spread of an opportunistic coral living or mutualistic species, and their introduction and pro- endosymbiont, Symbiodinium trenchii, from the Indo-Pacific liferation into new regions proceed without recognition. These into the Greater Caribbean, a region afflicted by human-related invasions may alter the composition of a host community and impacts including climate warming and environmental degra- affect the functional capacity of ecosystems (6, 7). Additional dation. As a symbiont, it increases the resilience of photosyn- climate warming and ecosystem degradation will likely facilitate thetic corals to environmental perturbation but may diminish increasing numbers of successful invasions, which may further the animal’s capacity to calcify and build reefs. This work ex- exacerbate negative ecological impacts (8). poses a critical need to better understand the consequences of Global change, especially ocean warming, continues to di- microbial introductions (even mutualistic species) on ecosystem minish the functional importance of reef corals by reducing their stability and function and raises questions about the long-term productivity, biodiversity, and capacity to precipitate calcium impact of new, but maladapted, symbioses on the productivity carbonate (9). The symbiotic dinoflagellates found in reef- of reef coral communities in the Atlantic Ocean. building corals (Symbiodinium) are crucial to the maintenance and photosynthetic productivity of coral reef ecosystems, thus Author contributions: D.T.P., D.C.W., R.T.S., R.I.-P., and T.C.L. designed research; D.T.P., D.C.W., R.T.S., and T.C.L. performed research; D.C.W., R.I.-P., and T.C.L. contributed new underscoring the importance of microbes and symbioses to reagents/analytic tools; D.T.P., D.C.W., R.T.S., and T.C.L. analyzed data; and D.T.P., D.C.W., ecosystem viability. Anomalous episodes of warm ocean tem- R.I.-P., and T.C.L. wrote the paper. peratures destabilize these mutualistic partnerships, resulting in The authors declare no conflict of interest. mass coral “bleaching” (i.e., symbiont expulsion) and mortality This article is a PNAS Direct Submission. over broad geographic expanses (10). Predicting the response of Data deposition: Source codes and data files for the analysis of observed pairwise genetic present day host–symbiont combinations to increasing anthro- difference (PWD), expected pairwise genetic difference under panmixia, and permu- pogenic warming and environmental degradation is a matter of tation test for departure from expected pairwise genetic difference among MLGs from datasets for S. trenchii populations in the Indian, Pacific, and Atlantic Oceans, as well considerable debate and involves broad speculation on whether as for S. “glynni” (type D1), type B7,typeA3,andC7 reported in this paper have been stress-tolerant symbionts might emerge to facilitate a rapid eco- deposited in the Dryad database, www.datadryad.org (doi: 10.5061/dryad.d4152). physiological response to changing conditions (11–14). However, 1To whom correspondence may be addressed. Email: [email protected] or [email protected]. it is unclear how symbiont replacement, or displacement (re- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ferred to as “switching” or “shuffling”), will progress in diverse 1073/pnas.1502283112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1502283112 PNAS Early Edition | 1of6 Downloaded by guest on September 29, 2021 were not native, motivating our population genetic investigation. little as 10 km contained distinct MLG assemblages of S. trenchii Indeed, detailed phylogenetic analyses are unable to distinguish (Table 1 and Fig. 1 B and C). Moreover, populations from Indo- S. trenchii in the Greater Caribbean from those in the Indo- Pacific locations contained a high diversity of alleles, including Pacific (15). Moreover, several other host-specialized Clade D many that were unique either to the eastern Indian or western Symbiodinium spp. often occur with S. trenchii in equatorial coral Pacific Oceans (Table 1). communities of the Indo-Pacific (20), but S. trenchii is the only S. trenchii species of Clade D found in the Atlantic. Finally, as mentioned Population Genetic Diversity of in the Greater Caribbean. S. trenchii Atlantic populations of S. trenchii were highly clonal and con- above, behaves opportunistically and can successfully = invade the colonies of many coral species experiencing physio- sisted of only a few MLGs ( clonal lineages) relative to the logical stress (analogous in some ways to “disturbed habitats”) number of samples analyzed (Table 1). Many clones were widely (16, 21). Therefore, we tested the hypothesis that populations of distributed throughout the Greater Caribbean basin, found in multiple locations separated by hundreds of kilometers (Figs. 1 Atlantic S. trenchii represent a recent invasion by examining in- D and E). The most notable of these common clones was the one terindividual genotypic diversity and divergence across the Indo- genotype comprising 42% of all samples (Figs. 1E and 2A). The Pacific and Greater Caribbean using high-resolution micro- distribution of this single clone (genotype α) (Fig. 1E) spanned satellite loci (22, 23). thousands of kilometers and was found in every Greater Carib- Results bean location, except the Gulf of Mexico (Fig. 1 D and E). There S. trenchii were several other common and widely distributed clones