Michael Stat

Functional diversity in coral–dinoflagellate symbiosis

Symbioses are widespread in nature and occur along a continuum from parasitism to mutualism. Coral–dinoflagellate symbioses are defined as mutualistic because both partners receive benefit from the association via the exchange of nutrients. This successful interaction underpins the growth and formation of coral reefs. The symbiotic dinoflagellate genus Symbiodinium is genetically diverse containing eight divergent lineages (clades A–H). Corals predominantly associate with clade C Symbiodinium and to a lesser extent with clades A, B, D, F, and G. Variation in the function and interactive physiology of different coral–dinoflagellate assemblages is virtually unexplored but is an important consideration when developing the contextual framework of factors that contribute to coral reef resilience. In this study, we present evidence that clade A Symbiodinium are functionally less beneficial to corals than the dominant clade C Symbiodinium and may represent parasitic rather than mutualistic symbionts. Our hypothesis is supported by (i) a significant correlation between the presence of Symbiodinium clade A and health-compromised coral; (ii) a phylogeny and genetic diversity within Symbiodinium that suggests a different evolutionary trajectory for clade A compared with the other dominant Symbiodinium lineages; and (iii) a significantly lower amount of carbon fixed and released by clade A in the presence of a coral synthetic host factor as compared with the dominant coral symbiont lineage, clade C. Collectively, these data suggest that along the symbiotic continuum the interaction between clade A Symbiodinium and corals may be closer to parasitism than mutualism.

Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics

Most studies on coral reefs have focused on shallow reef (< 30 m) systems due to the technical limitations of conducting scientific diving deeper than 30 m. Compared to their shallow-water counterparts, these mesophotic coral reefs (30-150 m) are understudied, which has slowed our broader understanding of the biodiversity, ecology, and connectivity of shallow and deep coral reef communities. We know that the light environment is an important component of the productivity, physiology, and ecology of corals, and it restricts the distribution of most species of coral to depths of 60 m or less. In the Bahamas, the coral Montastraea cavernosa has a wide depth distribution, and it is one of the most numerous corals at mesophotic depths. Using a range of optical, physiological, and biochemical approaches, the relative dependence on autotrophy vs. heterotrophy was assessed for this coral from 3 to 91 m. These measurements show that the quantum yield of PSII fluorescence increases significantly with depth for M. cavernosa while gross primary productivity decreases with depth. Both morphological and physiological photoacclimatization occurs to a depth of 91 m, and stable isotope data of the host tissues, symbionts, and skeleton reveal a marked decrease in productivity and a sharp transition to heterotrophy between 45 and 61 m. Below these depths, significant changes in the genetic composition of the zooxanthellae community, including genotypes not previously observed, occur and suggest that there is strong selection for zooxanthellae that are suited for survival in the light-limited environment where mesophotic M. cavernosa are occurring.

Clade D Symbiodinium in Scleractinian Corals: A “Nugget” of Hope, a Selfish Opportunist, an Ominous Sign, or All of the Above?

Clade D Symbiodinium are thermally tolerant coral endosymbionts that confer resistance to elevated sea surface temperature and bleaching to the host. The union between corals and clade D is thus important to management and coral conservation. Here, we review the diversity and biogeography of clade D Symbiodinium, factors linked to increasing abundances of clade D, and the benefits and drawbacks of associating with clade D for corals. We identify clade D Symbiodinium as uncommon pandemically distributed generalists found in higher abundances on reefs exposed to challenging sea surface temperatures and local stressors or with a history of bleaching. This distribution suggests that clade D Symbiodinium are mostly opportunistic endosymbionts, whereby they outcompete and replace optimal symbionts in health-compromised corals. We conclude by identifying research gaps that limit our understanding of the adaptive role clade D Symbiodinium play in corals and discuss the utility of monitoring clade D Symbiodinium as indicators of habitat degradation in coral reef ecosystems.

GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses

The genus Symbiodinium encompasses a group of unicellular, photosynthetic dinoflagellates that are found free living or in hospite with a wide range of marine invertebrate hosts including scleractinian corals. We present GeoSymbio, a hybrid web application that provides an online, easy to use and freely accessible interface for users to discover, explore and utilize global geospatial bioinformatic and ecoinformatic data on Symbiodinium–host symbioses. The novelty of this application lies in the combination of a variety of query and visualization tools, including dynamic searchable maps, data tables with filter and grouping functions, and interactive charts that summarize the data. Importantly, this application is hosted remotely or ‘in the cloud’ using Google Apps, and therefore does not require any specialty GIS, web programming or data programming expertise from the user. The current version of the application utilizes Symbiodinium data based on the ITS2 genetic marker from PCR‐based techniques, including denaturing gradient gel electrophoresis, sequencing and cloning of specimens collected during 1982–2010. All data elements of the application are also downloadable as spatial files, tables and nucleic acid sequence files in common formats for desktop analysis. The application provides a unique tool set to facilitate research on the basic biology of Symbiodinium and expedite new insights into their ecology, biogeography and evolution in the face of a changing global climate. GeoSymbio can be accessed at https://sites.google.com/site/geosymbio/.

Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals

Flexibility in biological systems is seen as an important driver of macro-ecosystem function and stability. Spatially constrained endosymbiotic settings, however, are less studied, although environmental thresholds of symbiotic corals are linked to the function of their endosymbiotic dinoflagellate communities. Symbiotic flexibility is a hypothesized mechanism that corals may exploit to adapt to climate change. This study explores the flexibility of the coral–Symbiodinium symbiosis through quantification of Symbiodinium ITS2 sequence assemblages in a range of coral species and genera. Sequence assemblages are expressed as an index of flexibility incorporating phylogenetic divergence and relative abundance of Symbiodinium sequences recovered from the host. This comparative analysis reveals profound differences in the flexibility of corals for Symbiodinium, thereby classifying corals as generalists or specifists. Generalists such as Acropora and Pocillopora exhibit high intra- and inter-species flexibility in their Symbiodinium assemblages and are some of the most environmentally sensitive corals. Conversely, specifists such as massive Porites colonies exhibit low flexibility, harbour taxonomically narrow Symbiodinium assemblages, and are environmentally resistant corals. Collectively, these findings challenge the paradigm that symbiotic flexibility enhances holobiont resilience. This underscores the need for a deeper examination of the extent and duration of the functional benefits associated with endosymbiotic diversity and flexibility under environmental stress.

COMPARISON OF ENDOSYMBIOTIC AND FREE‐LIVING SYMBIODINIUM (DINOPHYCEAE) DIVERSITY IN A HAWAIIAN REEF ENVIRONMENT

Many scleractinian corals must acquire their endosymbiotic dinoflagellates (genus Symbiodinium) anew each generation from environmental pools, and exchange between endosymbiotic and environmental pools of Symbiodinium (reef waters and sediments) has been proposed as a mechanism for optimizing coral physiology in the face of environmental change. Our understanding of the diversity of Symbiodinium spp. in environmental pools is poor by comparison to that engaged in endosymbiosis, which reflects the challenges of visualizing the genus against the backdrop of the complex and diverse micro‐eukaryotic communities found free‐living in the environment. Here, the molecular diversity of Symbiodinium living in the waters and sediments of a reef near Coconut Island, O‘ahu, Hawai‘i, sampled at four hourly intervals over a period of 5 d was characterized using a Symbiodinium‐specific hypervariable region of the chloroplast 23S. A comparison of Symbiodinium spp. diversity recovered from environmental samples with the endosymbiotic diversity in coral species that dominate the adjacent reef revealed limited overlap between these communities. These data suggest that the potential for infection, exchange, and/or repopulation of corals with Symbiodinium derived from the environment is limited at this location, a finding that is perhaps consistent with the high proportion of coral species in this geographic region that transmit endosymbionts from generation to generation.

Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef

Coral larvae acquire populations of the symbiotic dinoflagellate Symbiodinium from the external environment (horizontal acquisition) or inherit their symbionts from the parent colony (maternal or vertical acquisition). The effect of the symbiont acquisition strategy on Symbiodinium-host associations has not been fully resolved. Previous studies have provided mixed results, probably due to factors such as low sample replication of Symbiodinium from a single coral host, biogeographic differences in Symbiodinium diversity, and the presence of some apparently host-specific symbiont lineages in coral with either symbiont acquisition strategies. This study set out to assess the effect of the symbiont acquisition strategy by sampling Symbiodinium from 10 coral species (five with a horizontal and five with a vertical symbiont acquisition strategy) across two adjacent reefs in the southern Great Barrier Reef. Symbiodinium diversity was assessed using single-stranded conformational polymorphism of partial nuclear large subunit rDNA and denaturing gradient gel electrophoresis of the internal transcribed spacer 2 region. The Symbiodinium population in hosts with a vertical symbiont acquisition strategy partitioned according to coral species, while hosts with a horizontal symbiont acquisition strategy shared a common symbiont type across the two reef environments. Comparative analysis of existing data from the southern Great Barrier Reef found that the majority of corals with a vertical symbiont acquisition strategy associated with distinct species- or genus-specific Symbiodinium lineages, but some could also associate with symbiont types that were more commonly found in hosts with a horizontal symbiont acquisition strategy.

Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef

Shifts in the community of symbiotic dinoflagellates to those that are better suited to the prevailing environmental condition may provide reef-building corals with a rapid mechanism by which to adapt to changes in the environment. In this study, the dominant Symbiodinium in 10 coral species in the southern Great Barrier Reef was monitored over a 1-year period in 2002 that coincided with a thermal stress event. Molecular genetic profiling of Symbiodinium communities using single strand conformational polymorphism of the large subunit rDNA and denaturing gradient gel electrophoresis of the internal transcribed spacer 2 region did not detect any changes in the communities during and after this thermal-stress event. Coral colonies of seven species bleached but recovered with their original symbionts. This study suggests that the shuffling or switching of symbionts in response to thermal stress may be restricted to certain coral species and is probably not a universal feature of the coral–symbiont relationship.

Comparison of Endosymbiotic and Free-Living Symbiodinium (Dinophyceae) Diversity a Hawaiian Reef Environment. J Phycol

Many scleractinian corals must acquire their endosymbiotic dinoflagellates (genus Symbiodinium) anew each generation from environmental pools, and exchange between endosymbiotic and environmental pools of Symbiodinium (reef waters and sediments) has been proposed as a mechanism for optimizing coral physiology in the face of environmental change. Our understanding of the diversity of Symbiodinium spp. in environmental pools is poor by comparison to that engaged in endosymbiosis, which reflects the challenges of visualizing the genus against the backdrop of the complex and diverse micro‐eukaryotic communities found free‐living in the environment. Here, the molecular diversity of Symbiodinium living in the waters and sediments of a reef near Coconut Island, O‘ahu, Hawai‘i, sampled at four hourly intervals over a period of 5 d was characterized using a Symbiodinium‐specific hypervariable region of the chloroplast 23S. A comparison of Symbiodinium spp. diversity recovered from environmental samples with the endosymbiotic diversity in coral species that dominate the adjacent reef revealed limited overlap between these communities. These data suggest that the potential for infection, exchange, and/or repopulation of corals with Symbiodinium derived from the environment is limited at this location, a finding that is perhaps consistent with the high proportion of coral species in this geographic region that transmit endosymbionts from generation to generation.

Persistence and Change in Community Composition of Reef Corals through Present, Past, and Future Climates

The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past.