Oxidative stress, apoptosis activation and symbiosis disruption in giant clam Tridacna crocea under high temperature

Zhou, Zhi; Liu, Zhaoqun; Wang, Lingui; Luo, Jian; Hai-lang, LI

doi:10.1016/j.fsi.2018.10.033

Cited by 49 publications

(23 citation statements)

References 37 publications

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“…A 1.5°C temperature elevation over a 65-day period was sufficient to induce a significant reduction in symbiont density in small giant clams; no bleaching (even partial) was observed in control temperature clams. Our results support previous studies of corals and giant clams in which high temperature exposure led to sub-lethal bleaching ( 25 , 38 , 43 – 47 ); whether the cellular mechanisms of bleaching are conserved between corals and giant clams remains to be determined ( 38 , 48 ). For some coral species, resilience to heat stress is associated with a more flexible symbiotic association (i.e., the capacity to shift from one dominant Symbiodinium clade to another) ( 49 – 53 ).…”

Section: Discussionsupporting

confidence: 91%

“…( 36 , 37 ) have also been explored, yet few studies have looked at the mRNA level responses of multiple Symbiodinium clades and host systems in the same study. Furthermore, few physiological data and even fewer transcriptomic data are available for the high-temperature responses of the giant clam T. maxima and its symbionts (but see ( 31 , 38 )); these two published studies, though, only considered the response to an abrupt, rapid (and environmentally unrealistic) increase in temperature. Consequently, our understanding of the possible key drivers in high-temperature acclimation remains largely incomplete, despite its importance for generating better predictions of the impact of climate change on wild populations of giant clams ( 21 ).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Identifying conserved molecular mechanisms of thermo-acclimation in symbiotic organisms

Brahmi

et al. 2018

Preprint

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25 26 Seawater temperature rise in French Polynesia has repeatedly resulted in symbiosis breakdown 27 between giant clam (Tridacna maxima) and dinoflagellates (Symbiodinium spp.), particularly in 28 small individuals. Herein, we explored the physiological and gene expression responses of the 29 clam hosts and their photosynthetically active symbionts over a 65-day experiment in which 30 clams were exposed to either normal or environmentally relevant elevated seawater temperatures. 31These data were combined with publicly available data for both free-living Symbiodinium (clades 32 C1 and F) and Symbiodinium spp. in hospite with the coral Pocillopora damicornis. Gene module 33 preservation analysis revealed that the function of the symbionts' photosystem II was impaired at 34 high temperatures, and this response was conserved across all holobionts and Symbiodinium 35 clades examined. Similarly, activation of the phytohormone abscisic acid signaling and 36 epigenetics modulation appeared to be a key response mechanisms for symbionts in hospite with 37 giant clams exposed to high temperatures and also distinguish thermo-tolerant from thermo-38 sensitive Symbiodinium C1 phenotypes. 39 40MAIN TEXT 41 42Introduction 43 44Giant clams are mixotrophic organisms living in obligatory symbiosis with photosynthetic 45 dinoflagellates of the genus Symbiodinium (1, 2). Symbiodinium spp. associate not only with giant 46 clams, but with a diverse array of marine invertebrates, namely sponges, molluscs and cnidarians; 47 indeed, the coral-Symbiodinium symbiosis is the functional basis of all coral reefs (3). While in 48 scleractinian corals symbionts are located intracellularly, in giant clams they reside extracellularly 49 inside a tubular system called "Z-tubules," which are 1) found in the outer epithelium of the 50 mantle and 2) connected to the stomach (4). These in hospite dinoflagellates are known to provide 51 nutrients to the clam hosts via photosynthesis and may account for a major part of the clams' 52 energy needs (depending on the species and the life history stage) (5-9). The Symbiodinium genus 53 includes nine different clades with well characterized molecular and physiological differences 54 (10-12). One Symbiodinium clade, clade A (S. microadriaticum and S. fitti), has been recurrently 55 found in symbiosis with Tridacna maxima though members of clades C and D have been found in 56 clam tissues, as well (10,(13)(14)(15)(16)(17). Depending of the species, cladal representation of symbiont 57 types have been found to vary with individual size (mostly observed in T. squamosa), as well as 58 across environmental gradients (especially seawater temperatures) (15, 16). In French Polynesia, 59 eastern Tuamotu's archipelagos were historically characterized by high densities of small giant 60 clams (18)(19)(20). Recent mortality episodes and/or "bleaching" events in the Tuamotu Islands have, 61 however, been reported, including 1) a massive mortality event in 2009 that reduced the small 62 giant clam population by 90% at...

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Section: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Identifying conserved molecular mechanisms of thermo-acclimation in symbiotic organisms

Brahmi

et al. 2018

Preprint

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“…Indeed, by day 28, three GO categories were enriched that contained 108 upregulated genes involved in programmed cell death/apoptosis. The programmed cell death pathway has been observed before in the Symbiodiniaceae and their hosts under heat stress (e.g., Desalvo et al., 2008; Mohamed et al., 2016; Zhou, Liu, Wang, Luo, & Li, 2019) and could protect host cells (in symbiosis) and the remaining algal population under stress (Arnoult et al., 2002; Dunn, Thomason, Le Tissier, & Bythell, 2004; Huettenbrenner et al., 2003). Cell death by the WT@31 was observed through negative growth (decreases in cell number over time) (Chakravarti et al., 2017), and from day 28, photosynthetic efficiencies also started to decline (Figure 1c), further linking the upregulation of the programmed cell death pathway by the WT@31 and the decline in overall health of the cells.…”

Section: Resultsmentioning

confidence: 81%

Gene regulation underpinning increased thermal tolerance in a laboratory‐evolved coral photosymbiont

Chakravarti

Buerger

Levin³

et al. 2020

Molecular Ecology

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Small increases in ocean temperature can disrupt the obligate symbiosis between corals and dinoflagellate microalgae, resulting in coral bleaching. Little is known about the genes that drive the physiological and bleaching response of algal symbionts to elevated temperature. Moreover, many studies to‐date have compared highly divergent strains, making it challenging to accredit specific genes to contrasting traits. Here, we compare transcriptional responses at ambient (27°C) and bleaching‐relevant (31°C) temperatures in a monoclonal, wild‐type (WT) strain of Symbiodiniaceae to those of a selected‐strain (SS), derived from the same monoclonal culture and experimentally evolved to elevated temperature over 80 generations (2.5 years). Thousands of genes were differentially expressed at a log fold‐change of >8 between the WT and SS over a 35 days temperature treatment period. At 31°C, WT cells exhibited a temporally unstable transcriptomic response upregulating genes involved in the universal stress response such as molecular chaperoning, protein repair, protein degradation and DNA repair. Comparatively, SS cells exhibited a temporally stable transcriptomic response and downregulated many stress response genes that were upregulated by the WT. Among the most highly upregulated genes in the SS at 31°C were algal transcription factors and a gene probably of bacterial origin that encodes a type II secretion system protein, suggesting interactions with bacteria may contribute to the increased thermal tolerance of the SS. Genes and functional pathways conferring thermal tolerance in the SS could be targeted in future genetic engineering experiments designed to develop thermally resilient algal symbionts for use in coral restoration and conservation.

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“…However, taxa able to grow their shells over water temperature changes of >12 °C are not uncommon (97,102). Following tank experiments short-term temperature rises by up to 6 °C can induce death of the symbiotic zooxanthellae and bleaching [ 120 , 121 ], without presenting a major metabolic stress for the bivalve host [ 120 ]. Furthermore, as discussed above, the annual ΔT amplitude of the Tethyan shallow water might have been lower than 11 °C, considering the effect of the seasonally changing δ 18 O w on the δ 18 O shell records of the rudists.…”

Section: Discussionmentioning

confidence: 99%

Paleoceanography of the Late Cretaceous northwestern Tethys Ocean: Seasonal upwelling or steady thermocline?

Walliser¹,

Schöne²

2020

PLoS ONE

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In this study we attempted to assess whether seasonal upwelling or a steady thermocline persisted at the western margin of the Tethys Ocean during the late Turonian-early Coniacian interval. For this scope, we employed novel and published stable oxygen isotope (δ 18 O) data of various organisms (bivalves, bivalves, brachiopods, fish and belemnites). New seasonally resolved temperature estimates were based on the δ 18 O record of sequentially sampled inoceramid (Inoceramus sp.) and rudist (Hippurites resectus) shells from the Scaglia Rossa and Gosau deposits of northern Italy and western Austria, respectively. Diagenetic screening was performed using reflected light, cathodoluminescence (CL), scanning electron microscopy (SEM) and stable isotope analysis. Originally preserved δ 13 C and δ 18 O values were used to characterize the lifestyle of the bivalves and detect vital effects that could have biased oxygen isotope-based temperature reconstructions. Inoceramid δ 18 O values provide-for the first time-information on temperatures of Tethyan benthic waters, which were, on average, 14.4 ± 0.6˚C and fluctuated seasonally within a range of less than 2˚C. Such a thermal regime is in line with the temperatures postulated for late Turonian boreal water masses and support the existence of a cold water supply from the North Atlantic to the Tethyan bottom. Bottom cooling, however, did not affect the shallow water environment. In fact, the rudist-based temperature estimates for shallow water environment revealed a mean annual range of 11˚C, between 24 and 35˚C (assuming a seasonally constant δ18O w = 1.0 ‰), which are among the warmest temperatures recorded over the entire Late Cretaceous. Our findings, thus, suggest a strong thermal and food web decoupling between the two environments. The absence of a seasonal vertical homogenization of different water bodies suggests the existence of a steady thermocline and, therefore, contrasts with the presence of an active coastal upwelling in the region as hypothesized by previous authors.

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Oxidative stress, apoptosis activation and symbiosis disruption in giant clam Tridacna crocea under high temperature

Cited by 49 publications

References 37 publications

Identifying conserved molecular mechanisms of thermo-acclimation in symbiotic organisms

Identifying conserved molecular mechanisms of thermo-acclimation in symbiotic organisms

Gene regulation underpinning increased thermal tolerance in a laboratory‐evolved coral photosymbiont

Paleoceanography of the Late Cretaceous northwestern Tethys Ocean: Seasonal upwelling or steady thermocline?

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