doi: 10.1038/s42003-023-05350-8.
Genes possibly related to symbiosis in early life stages of Acropora tenuis inoculated with Symbiodinium microadriaticum
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- PMCID: PMC10584924
- DOI: 10.1038/s42003-023-05350-8
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Genes possibly related to symbiosis in early life stages of Acropora tenuis inoculated with Symbiodinium microadriaticum
Yuki Yoshioka et al. Commun Biol..
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Abstract
Due to the ecological importance of mutualism between reef-building corals and symbiotic algae (Family Symbiodiniaceae), various transcriptomic studies on coral-algal symbiosis have been performed; however, molecular mechanisms, especially genes essential to initiate and maintain 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 symbiosis-related genes. Genes involved in immune regulation, protection 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 possible 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 among coral lineages.
© 2023. Springer Nature Limited.
Conflict of interest statement
The authors declare no competing interests.
Figures
a A schematic illustration of the experimental design. Primary polyps were maintained at a concentration of ~5 individuals/well of a 24-well multi-plate. 200,000 algal cells of Smic were added to the treatment group. Two days after addition of algae, artificial seawater (ASW) was replaced, and 200,000 algal cells of Smic were reintroduced. The process of ASW exchange and algal addition was repeated every two days until 8 days post-inoculation (dpi). Subsequently, only ASW exchange was conducted until 20 dpi. RNA extraction was conducted for each well containing ~5 primary polyps at 10 and 20 dpi. One well containing ~5 individuals was considered one replicate. See Method for details.b Total numbers of up- and downregulated DEGs in each dpi are shown on the left. Each row contains elements represented by black circles. The line connecting elements indicates DEGs shared between samples. Vertical bars with blue and/or red indicate results of DEG annotation (BLAST searches against the Swiss-Prot database) belonging to each element. Gene ID, Swiss-Prot annotation, and Pfam domain of DEGs are provided in Supplementary Data 1.
a A Venn-diagram of the number of DEGs in planula larvae and primary polyps inoculated with Smic.b Numbers of acquired Smic cells per coral. Lines indicate average ± SE of acquired Smic cells in primary polyps and planula larvae. Raw data are shown in Supplementary Table 1.c Heatmap showing log2-transformed fold change of 15 possible symbiosis-related DEGs whose expression levels correlated with numbers of algae in corals. Expression levels were compared to corresponding controls (apo-symbiotic larvae or primary polyps). Asterisks indicate significant differences of gene expression levels (FDR < 0.05) compared with controls. NA indicates that calculations were not possible due to very low expression in control samples.
Possible protein name, gene name, and gene ID are shown at the left of each sequence (Left). Short names of evolutionary conserved protein domains (Pfams) are shown in or around each domain. Amino acid sequence length is shown at the right of each sequence. Symbols (†, §, and ¶) after parentheses indicate that protein domain compositions are completely conserved, partially conserved, or not conserved, compared with homologs of humans or yeasts. Numbers of duplicates are shown in the heatmap (Right). Tree topology shows phylogenetic relationships among species inferred by OrthoFinder. *1 and *2 indicate that they belong to the same gene family. Abbreviation: Aten,A. tenuis; Adig,A. digitifera; Amil,A. millepora;, Mcac,M. cactus; Meff,M. efflorescens; Astr,Astreopora myriophthalma; Paus,Porites australiensis; SpisS. pistillata; Ofav,O. faveolata; Pdam,Pocillopora damicornis; Edia,Exaiptasia diaphana; Nvec,Nematostella vectensis.
The symbiotic algae Smic (S. microadriaticum) is surrounded by the symbiosome, the organelle in which a symbiont resides. Antioxidant response regulatory genes (Chac,Pxd,Psap-like, andMmp-like) are expected to protect against oxidative stress caused by reactive oxygen species produced in coral mitochondria and/or plastids of algal symbionts. Transporter genes (SLC2A8,SLC26A2, andNPC2) are likely involved in metabolic interactions of sugars, lipids, and sulfates between symbiotic partners, Ligand-like genes (AnNLL andGrn-like) are predicted to be involved in immune regulation for maintenance of coral-algal symbioses.
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