Worldwide Occurrence and Activity of the Reef-Building Coral Symbiont Symbiodinium in the Open Ocean

Decelle, Johan; Carradec, Quentin; Pochon, Xavier; Henry, Nicolas; Romac, Sarah; Mahé, Frédéric; Dunthorn, Micah; Kourlaiev, Artem; Voolstra, Christian R.; Wincker, Patrick; Vargas, Colomban de

doi:10.1016/j.cub.2018.09.024

Cited by 51 publications

(43 citation statements)

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“…This scenario is further supported by the fact that Phaeocystis cells cannot be grown after the symbiotic stage, do not divide within their host, and are very likely digested at the end of the life cycle of their host [7]. Available evidence suggests that the degree of host control seems to be less pronounced in other photosymbioses (e.g., reef invertebrates, foraminiferans) since the algal symbiont can divide within its host and can be grown in culture or survive in natural seawater after the symbiotic stage [6,54]. In an evolutionary context, similar traits found in symbiotic Phaeocystis have been reported in Paulinella chromatophora, a recent primary endosymbiosis, where photosynthetic organelles (chromatophores) are 15-20 times larger than in free-living cyanobacteria [55,56].…”

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confidence: 99%

Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

et al. 2019

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Section: Discussionmentioning

confidence: 99%

Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

et al. 2019

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“…Certain members of family Symbiodiniaceae are known to exist both in a free‐living state (Coffroth, Lewis, Santos, & Weaver, ; Decelle et al, ) and as endosymbionts within cnidarian hosts (Stambler, ). Our transcriptome analysis on cultured and in hospite Breviolum minutum highlights how distinct the two life stages are, while the clustering of biological replicates is indicative of robustness in our analysis (Figure ).…”

Section: Discussionmentioning

confidence: 99%

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Maor-Landaw

Oppen

McFadden

2019

Ecology and Evolution

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Coral-dinoflagellate symbiosis underpins the evolutionary success of corals reefs. Successful exchange of molecules between the cnidarian host and the Symbiodiniaceae algae enables the mutualistic partnership. The algae translocate photosynthate to their host in exchange for nutrients and shelter. The photosynthate must traverse multiple membranes, most likely facilitated by transporters. Here, we compared gene expression profiles of cultured, free-living Breviolum minutum with those of the homologous symbionts freshly isolated from the sea anemone Exaiptasia diaphana, a widely used model for coral hosts. Additionally, we assessed expression levels of a list of candidate host transporters of interest in anemones with and without symbionts. Our transcriptome analyses highlight the distinctive nature of the two algal life stages, with many gene expression level changes correlating to the different morphologies, cell cycles, and metabolisms adopted in hospite versus free-living.Morphogenesis-related genes that likely underpin the metamorphosis process observed when symbionts enter a host cell were up-regulated. Conversely, many downregulated genes appear to be indicative of the protective and confined nature of the symbiosome. Our results emphasize the significance of transmembrane transport to the symbiosis, and in particular of ammonium and sugar transport. Further, we pinpoint and characterize candidate transporters-predicted to be localized variously to the algal plasma membrane, the host plasma membrane, and the symbiosome membrane-that likely serve pivotal roles in the interchange of material during symbiosis.Our study provides new insights that expand our understanding of the molecular exchanges that underpin the cnidarian-algal symbiotic relationship. K E Y W O R D S Breviolum minutum, Exaiptasia diaphana, free-living, in hospite, symbiosis, transporters S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Maor-Landaw K, van Oppen MJH, McFadden GI. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae).

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“…However, colonies of several coral species exhibit no changes in their Symbiodiniaceae communities during exposure to variable temperatures or bleaching stress (McGinley et al, ; Stat, Loh, LaJeunesse, Hoegh‐Guldberg, & Carter, ; Thornhill, LaJeunesse, Kemp, Fitt, & Schmidt, ). These contradictory observations have been linked to evolutionary differences among host and symbiont species in their capacity to associate with each other (Aranda et al, ; Putnam, Stat, Pochon, & Gates, ), inferior nutrition from novel symbionts (Cantin, van Oppen, Willis, Mieog, & Negri, ; Cunning, Silverstein, & Baker, ; Little, van Oppen, & Willis, ; Rädecker et al, ) and the environmental availability of Symbiodiniaceae diversity (Cumbo, Baird, & van Oppen, ; Cunning, Yost, Guarinello, Putnam, & Gates, ; Decelle et al, ). Alternatively, the low taxonomic and quantitative resolution of early molecular identification approaches may have prevented the detection of fine‐scale changes in Symbiodiniaceae communities (Boulotte et al, ; Quigley et al, ; Ziegler, Eguíluz, Duarte, & Voolstra, ), or the warming levels experienced by corals may not have been strong enough to drive community changes.…”

Section: Introductionmentioning

confidence: 99%

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

et al. 2020

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Reef‐building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host‐specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching‐resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co‐evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.

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Worldwide Occurrence and Activity of the Reef-Building Coral Symbiont Symbiodinium in the Open Ocean

Cited by 51 publications

References 48 publications

Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

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