Larval transcriptomic responses of a stony coral, Acropora tenuis, during initial contact with the native symbiont, Symbiodinium microadriaticum

Yoshioka, Yuki; Yamashita, Hiroshi; Suzuki, Go; Shinzato, Chuya

doi:10.1038/s41598-022-06822-3

Cited by 10 publications

(10 citation statements)

References 70 publications

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“…This flexibility in initial uptake by coral recruits relative to adults has been demonstrated in a number of coral species (e.g., Ali et al, 2019 ; Chan et al, 2019 ; Coffroth et al, 2001 ; Gómez‐Cabrera et al, 2008 ; Poland et al, 2013 ), and several, non‐exclusive, hypotheses have been proposed to explain this pattern. The tendency for newly settled corals to harbor a distinct and/or more diverse array of symbiont types than their adult conspecifics may be the byproduct of an undeveloped immune system in recruits (Frank et al, 1997 ; Nozawa & Loya, 2005 ; Puill‐Stephan et al, 2012 ) or the suppression of the host immune response by the symbionts (Jacobovitz et al, 2021 ; Mansfield & Gilmore, 2019 ; Schnitzler & Weis, 2010 ; Voolstra et al, 2009 ; Yoshioka et al, 2022 ). Then, as recruits age and presumably as the immune system develops, recruits are less likely to take up new symbiont genotypes (McIlroy & Coffroth, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Genetic structure of dinoflagellate symbionts in coral recruits differs from that of parental or local adults

Coffroth

Leigh

McIlroy

et al. 2022

Ecology and Evolution

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The symbiotic relationship between dinoflagellate algae in the family Symbiodiniaceae and scleractinian corals forms the base of the tropical reef ecosystem. In scleractinian corals, recruits acquire symbionts either “vertically” from the maternal colony or initially lack symbionts and acquire them “horizontally” from the environment. Regardless of the mode of acquisition, coral species and individual colonies harbor only a subset of the highly diverse complex of species/taxa within the Symbiodiniaceae. This suggests a genetic basis for specificity, but local environmental conditions and/or symbiont availability may also play a role in determining which symbionts within the Symbiodiniaceae are initially taken up by the host. To address the relative importance of genetic and environmental drivers of symbiont uptake/establishment, we examined the acquisition of these dinoflagellate symbionts in one to three‐month‐old recruits of Orbicella faveolata to compare symbiont types present in recruits to those of parental populations versus co‐occurring adults in their destination reef. Variation in chloroplast 23S ribosomal DNA and in three polymorphic microsatellite loci was examined. We found that, in general, symbiont communities within adult colonies differed between reefs, suggesting that endemism is common among symbiont populations of O. faveolata on a local scale. Among recruits, initial symbiont acquisition was selective. O. faveolata recruits only acquired a subset of locally available symbionts, and these generally did not reflect symbiont populations in adults at either the parental or the outplant reef. Instead, symbiont communities within new recruits at a given outplant site and region tended to be similar to each other, regardless of parental source population. These results suggest temporal variation in the local symbiont source pool, although other possible drivers behind the distinct difference between symbionts within O. faveolata adults and new generations of recruits may include different ontogenetic requirements and/or reduced host selectivity in early ontogeny.

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Section: Discussionmentioning

confidence: 99%

Genetic structure of dinoflagellate symbionts in coral recruits differs from that of parental or local adults

Coffroth

Leigh

McIlroy

et al. 2022

Ecology and Evolution

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“…For Montipora , eggs, sperm, planula larvae (1 and 4 d post-fertilization) were collected and preserved with TRIzol reagent (Thermo Fisher Scientific) at -80℃ until use. Total RNA was extracted from preserved eggs, sperm, and planula larvae as in Yoshioka et al [ 56 ]. KAPA RNA HyperPrep Kits (Kapa Biosystems) and MGIEasy RNA Directional Library Prep Sets (MGI) were used for total RNA and mRNA sequencing library preparation, and each library was sequenced on a NovaSeq 6000 in 150-bp paired-end and a DNBSEQ-G400RS (MGI) in 100-bp paired-end mode.…”

Section: Methodsmentioning

confidence: 99%

Comparative genomics highlight the importance of lineage-specific gene families in evolutionary divergence of the coral genus, Montipora

Yoshioka

Suzuki²,

Zayasu

et al. 2022

BMC Ecol Evo

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Background Scleractinian corals of the genus Montipora (Anthozoa, Cnidaria) possess some unusual biological traits, such as vertical transmission of algal symbionts; however, the genetic bases for those traits remain unknown. We performed extensive comparative genomic analyses among members of the family Acroporidae (Montipora, Acropora, and Astreopora) to explore genomic novelties that might explain unique biological traits of Montipora using improved genome assemblies and gene predictions for M. cactus, M. efflorescens and Astreopora myriophthalma. Results We obtained genomic data for the three species of comparable high quality to other published coral genomes. Comparative genomic analyses revealed that the gene families restricted to Montipora are significantly more numerous than those of Acropora and Astreopora, but their functions are largely unknown. The number of gene families specifically expanded in Montipora was much lower than the number specifically expanded in Acropora. In addition, we found that evolutionary rates of the Montipora-specific gene families were significantly higher than other gene families shared with Acropora and/or Astreopora. Of 40 gene families under positive selection (Ka/Ks ratio > 1) in Montipora, 30 were specifically detected in Montipora-specific gene families. Comparative transcriptomic analysis of early life stages of Montipora, which possesses maternally inherited symbionts, and Acropora, which lacks them, revealed that most gene families continuously expressed in Montipora, but not expressed in Acropora do not have orthologs in Acropora. Among the 30 Montipora-specific gene families under positive selection, 27 are expressed in early life stages. Conclusions Lineage-specific gene families were important to establish the genus Montipora, particularly genes expressed throughout early life stages, which under positive selection, gave rise to biological traits unique to Montipora. Our findings highlight evolutionarily acquired genomic bases that may support symbiosis in these stony corals and provide novel insights into mechanisms of coral-algal symbiosis, the physiological foundation of coral reefs.

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“…Innate immunity system is important in cnidarian symbioses 24,41 . Cnidarian hosts suppress their immune response when they are inoculated with symbiotic algae 26,35 . Progranulin, encoded by Grn, is a multifunctional protein that modulates immune responses in mammals, such as blocking TNFinduced immune responses 75 .…”

Section: Possible Oxidative Stress Prevention and Immune Control Duri...mentioning

confidence: 99%

Possible core symbiosis-related genes in early life stages of Acropora tenuis inoculated with Symbiodinium microadriaticum

Chiu¹,

Uchida²,

Yamashita³

et al. 2023

Preprint

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Due to the ecological importance of mutualisms between reef-building corals and symbiotic algae (Family Symbiodiniaceae), various transcriptomic studies on coral-algal symbiosis have been performed; however, molecular mechanisms, especially essential genes in these symbioses remain unknown. We investigated transcriptomic responses of Acropora tenuis to inoculation with the native algal symbiont, Symbiodinium microadriaticum, during early life stages, and identified possible “core” symbiosis-related genes. Genes involved in immune suppression, defense against oxidative stress, and metabolic interactions between partners are particularly important for symbiosis during Acropora early life stages. In addition, molecular phylogenetic analysis revealed that some core symbiosis-related genes originated by gene duplication in the Acropora lineage, suggesting that gene duplication may have been the driving force to establish stable mutualism in Acropora, and that symbiotic molecular mechanisms may vary depending on each coral lineage.

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Larval transcriptomic responses of a stony coral, Acropora tenuis, during initial contact with the native symbiont, Symbiodinium microadriaticum

Cited by 10 publications

References 70 publications

Genetic structure of dinoflagellate symbionts in coral recruits differs from that of parental or local adults

Genetic structure of dinoflagellate symbionts in coral recruits differs from that of parental or local adults

Comparative genomics highlight the importance of lineage-specific gene families in evolutionary divergence of the coral genus, Montipora

Possible core symbiosis-related genes in early life stages of Acropora tenuis inoculated with Symbiodinium microadriaticum

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