Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient

Wall, Christopher B.; Kaluhiokalani, Mario; Popp, Brian N.; Donahue, Megan J.; Gates, Ruth D.

doi:10.1038/s41396-019-0570-1

Cited by 64 publications

(63 citation statements)

References 92 publications

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“…Moreover, the translocated fragments, which have lower TP, are still grouping with the shallow colonies in the PCA and do not form a separate group, meaning predation is not representing a significant portion of their carbon source or that due to the carbon cycling the essential amino-acids originate from the symbiont regardless of predation. It seems that the existing assumption, according to which the differences in carbon isotope fractionation between mesophotic and shallow corals are due to different symbiont genera (Ezzat et al, 2017;Wall et al, 2020), in our case, is not applicable. That is since our translocated fragments have changed less than 20% of their symbionts to S. microadriaticum (inhabiting shallow corals) and retained C. goreaui (inhabiting mesophotic corals).…”

Section: Discussionmentioning

confidence: 60%

“…Constraining the nitrogen isotopic baseline, or isotopic composition of primary producers at the base of an ecosystem can be complicated and may be difficult or impossible in many environments (Popp et al, 2007). This problem seems to be significant in corals, where anticipated differences between corals with predicted differing TPs are not evident or are hard to separate from other forces that change δ 15 N (Houlbrèque and Ferrier-Pagès, 2009;Nahon et al, 2013;Fox et al, 2019;Wall et al, 2020). McClelland and Montoya (2002) were the first to examine the amino acids compound-specific stable isotope (AA-CSIA) in the relationship between phytoplankton and their consumer zooplankton in a controlled laboratory setting.…”

Section: Introductionmentioning

confidence: 99%

“…Hence, a simple comparison between shallow and mesophotic S. pistillata colonies is a comparison between the same host species, but with a different symbiont. Therefore, it is not possible to attribute observed differences in holobiont physiology to the adaptation of either the host or the symbiont, as they may simply arise from the different symbiont genera ( Wall et al., 2020 ). In the present work, stepwise transplantation of S. pistillata from 60 to 5 m reefs was conducted.…”

Section: Introductionmentioning

confidence: 99%

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Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata

et al. 2020

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Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ15N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a, lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.

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Section: Discussionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata

et al. 2020

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“…Given that the coral M. capitata is known to be dominated by two genetically and physiologically contrasting Symbiodiniaceae, Cladocopium sp. and Durusdinium glynnii (Cunning et al, 2016; Wall, Kaluhiokalani, Popp, Donahue, & Gates, 2020), we predicted (H3) that holobionts harboring heat-tolerant D. glynnii would show higher immune and antioxidant responses linked to greater bleaching resistance. To test these hypotheses, we measured bleaching severity and recovery at each location using benthic surveys and measured coral traits in coral fragments, including: physiological measurements of cellular bleaching magnitude (symbiont density, areal- and cell-specific chlorophyll a , holobiont total protein and total biomass), and completed enzymatic assays for mechanisms contributing to bleaching resistance through coral host antioxidant capacity (peroxidase, catalase, superoxide dismutase), and the host immune response of the melanin cascade (prophenoloxidase, melanin).…”

Section: Introductionmentioning

confidence: 89%

Shifting Baselines: Physiological legacies contribute to the response of reef coral to frequent heat waves

Wall

Ricci

Wen

et al. 2020

Preprint

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Global climate change is altering coral reef ecosystems. Notably, marine heat waves are producing widespread coral bleaching events with increased frequency, with projections for annual bleaching events on many reefs by mid-century. The response of corals to elevated seawater temperatures is, however, influenced by a combination of environmental legacies, the biology of the host, and the resident symbiont community, each of which have the capacity to modulate resistance and resilience to environmental stress. It is critical, therefore, to evaluate the potential for shifting physiological and molecular baselines driven by these factors in back-toback in situ bleaching (and recovery) events given the potential for mortality of corals in response to episodic bleaching episodes and increased ocean warming. Here, we use the regional bleaching events of 2014 and 2015 in the Hawaiian Islands and subsequent recovery periods to test the hypothesis that coral multivariate responses (physiotypes) differed in back-to-back bleaching events, modulated by both environmental histories and symbiotic partnerships (Symbiodiniaceaea). Bleaching severity was greater in the first-bleaching event, and concomitantly, environmental history effects were more pronounced. Melanin, an immune cytotoxic response, provided an initial defense during the first-bleaching event and primed antioxidant activity, which peaked in the second-bleaching event. While magnitude of bleaching differed, immune response patterns were shared among corals harboring heat-sensitive and heattolerant Symbiodiniaceae. This supports a pattern of increased constitutive immunity in corals during repeat bleaching events, demonstrated by greater specialized enzymes (catalase, superoxide dismutase, peroxidase) and attenuated melanin synthesis. This study demonstrates bleaching events trigger cumulative and interactive physiotypes driven by environmental legacy and cellular memory. Quantifying baseline and altered coral physiotypes (multivariate

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“…In return, Symbiodiniaceae supply the coral host with photosynthates and other organic nutrients, which can meet up to 95% of the corals' energy requirements (Muscatine and Porter, 1977). The mutual nutrient exchange determines the stability and maintenance of the coral-Symbiodiniaceae symbiosis (Liu et al, 2018;Wall et al, 2020). However, it has been considered that the coral-Symbiodiniaceae symbiosis is vulnerable to environmental changes, especially for elevated seawater temperature (Vidal-Dupiol et al, 2011).…”

Section: Introductionmentioning

confidence: 99%