Broadcast Spawning Coral Mussismilia hispida Can Vertically Transfer its Associated Bacterial Core

Abstract

The hologenome theory of evolution (HTE), which is under fierce debate, presupposes that parts of the microbiome are transmitted from one generation to the next [vertical transmission (VT)], which may also influence the evolution of the holobiont. Even though bacteria have previously been described in early life stages of corals, these early life stages (larvae) could have been inoculated in the water and not inside the parental colony (through gametes) carrying the parental microbiome. How Symbiodinium is transmitted to offspring is also not clear, as only one study has described this mechanism in spawners. All other studies refer to incubators. To explore the VT hypothesis and the key components being transferred, colonies of the broadcast spawner species Mussismilia hispida were kept in nurseries until spawning. Gamete bundles, larvae and adult corals were analyzed to identify their associated microbiota with respect to composition and location. Symbiodinium and bacteria were detected by sequencing in gametes and coral planula larvae. However, no cells were detected using microscopy at the gamete stage, which could be related to the absence of those cells inside the oocytes/dispersed in the mucus or to a low resolution of our approach. A preliminary survey of Symbiodinium diversity indicated that parental colonies harbored Symbiodinium clades B, C and G, whereas only clade B was found in oocytes and planula larvae [5 days after fertilization (a.f.)]. The core bacterial populations found in the bundles, planula larvae and parental colonies were identified as members of the genera Burkholderia, Pseudomonas, Acinetobacter, Ralstonia, Inquilinus and Bacillus, suggesting that these populations could be vertically transferred through the mucus. The collective data suggest that spawner corals, such as M. hispida, can transmit Symbiodinium cells and the bacterial core to their offspring by a coral gamete (and that this gamete, with its bacterial load, is released into the water), supporting the HTE. However, more data are required to indicate the stability of the transmitted populations to indicate whether the holobiont can be considered a unit of natural selection or a symbiotic assemblage of independently evolving organisms.

Specific plasmid patterns and high rates of bacterial co‐occurrence within the coral holobiont

“… Members of the bacterial core that are vertically transmitted in M. hispida, as described by Leite et al., . …”

“…(a) All significant interactions, involving 38 OTUs, sorted by class and densely interconnected regions, Cluster 1 (b), Cluster 2 (c), and Cluster 3 (d). The core bacteriome members vertically transferred (Leite et al., ) are highlighted in yellow…”

“…Our main findings indicate that key groups of bacteria, that is, Proteobacteria, followed by Firmicutes, mainly represented by members of Rhodobacteraceae and the genera Pseudomonas and Bacillus associated with M. hispida , were present in the coral mucus. These dominant groups and members of the entire M. hispida microbial core have also been described as being vertically transmitted from parent to offspring in the same coral species (Leite et al., ). In addition, this core microbiome and some other groups in the mucus bacteriome have a positive relationship of co‐occurrence, especially the families Desulfovibrionaceae and Flavobacteriaceae, the genera Pseudoalteromonas and Arcobacter , and Rugeria and other members of Rhodobacteraceae, suggesting that these microorganisms could be selected by the holobiont.…”

“…It has been proposed that important mechanisms associated with the holobiont, that is, the host and its associated microbial community (Margulis & Fester, ), can be regulated through microbiome shuffling (i.e., shifts in microbial abundance) and/or switching (i.e., acquisition of the microbial strains from the surrounding environment) (reviewed in Webster & Reusch, ). The acquired microorganisms could also be passed on from parental to offspring generations (Leite et al., ; Padilla‐Gamiño, Pochon, Bird, Concepcion, & Gates, ). This microbiome‐mediated transgenerational acclimatization (MMTA) (proposed by Webster & Reusch, ) could lead to the rapid adaptation (and evolution) of corals to adverse environmental conditions.…”

Microbiome engineering: enhancing climate resilience in corals

“…Conversely, Mussismilia hispida , also a broadcast spawner, has been found to vertically transfer prokaryotes from parental mucus to gametes prior to spawning (Leite et al . ). Gaining a better understanding of prokaryote transmission in a range of coral species, along with assessing the maintenance of these prokaryotic associations (eg whether any host or microbe‐controlled cellular mechanism is at work) through time or across generations, may help to elucidate microbiome stability and identify better BMC targets for ME trials.…”