Diversity and dynamics of multiple symbionts contribute to early development of broadcast spawning reef-building coral <i>Dipsastraea veroni</i>

Sexual reproduction and recruitment enhance the genetic diversity and evolution of reef-building corals for population recovery and coral reef conservation under climate change. However, new recruits are vulnerable to physical changes and the mechanisms of symbiosis establishment remain poorly understood. Here, <i>Dipsastraea veroni</i>, a broadcast spawning hermaphrodite reef-building coral, was subjected to settlement and juvenile growth in flow-through <i>in situ</i> seawater at 27.93 ± 0.96°C. Symbiosis of Symbiodiniaceae, bacteria, and/or archaea by horizontal acquisition and/or hypothetical vertical transmission through the mucus with symbionts from the parent appears to be a heritable process of selection and adaptation in <i>D. veroni</i> at the egg, larva, juvenile (5 days post settlement, d p.s. and 32 d p.s.) stages. Symbiodiniaceae was dominated by the genera <i>Cladocopium</i>, <i>Durusdinium</i>, <i>Symbiodinium,</i> with increasing relative abundance of <i>Durusdinium</i> at 5 d p.s. and <i>Symbiodinium</i> at 32 d p.s. Mixed acquisition of the dominant phyla Pseudomonadota, Bacteroidota, Cyanobacteriota, Bacillota, Planctomycetota, and Actinomycetota in egg, larva, and/or juvenile showed a winnowing and regulated bacterial diversity and dynamics, resulting in stage-abundant orders Pseudomonadales and Bacillales in egg and Rhodobacterales, Rhodospirillales, Cyanobacteria, and Cyanobacteriales in larva and/or juvenile. The photoautotrophic Chloroflexales, Cyanobacteriales, and Chlorobiales were abundant in adults. The stable archaeal community contained predominant Crenarchaeota, Halobacterota, Nanoarchaeia Thermoplasmatota, and eight rare phyla, with increased relative abundance of the genera <i>Bathyarchaeota</i>, <i>Candidatus_Nitrosopumilus</i>, <i>Candidatus_Nitrocosmicus</i>, <i>Nitrosarchaeum</i>, <i>Candidatus_Nitrosotenuis</i>, <i>Candidatus_Nitrosopelagicus</i>, <i>Cenarchaeum</i>, <i>Haladaptatus</i>, <i>Halogranum</i>, <i>Halolamina,</i> and <i>Woesearchaeales</i> and <i>GW2011-AR15</i> in juveniles. All results revealed flexible symbiotic mechanisms in <i>D. veroni</i> during early ontogeny for coral survival and evolution.IMPORTANCEFlexible symbioses of Symbiodiniaceae, bacteria, and archaea appear to be a heritable process of selection and adaptation in <i>Dipsastraea veroni</i> in the field, benefiting early coral development and facilitating coral population recovery and reef conversation.