Microbiomes of the Sydney Rock Oyster are acquired through both vertical and horizontal transmission

Abstract

Background The term holobiont is widely accepted to describe animal hosts and their associated microorganisms. The genomes of all that the holobiont encompasses, are termed the hologenome and it has been proposed as a unit of selection in evolution. To demonstrate that natural selection acts on the hologenome, a significant portion of the associated microbial genomes should be transferred between generations. Using the Sydney Rock Oyster (Saccostrea glomerata) as a model, we tested if the microbes of this broadcast spawning species could be passed down to the next generation by conducting single parent crosses and tracking the microbiome from parent to offspring and throughout early larval stages using 16S rRNA gene amplicon sequencing. From each cross, we sampled adult tissues (mantle, gill, stomach, gonad, eggs or sperm), larvae (D-veliger, umbo, eyed pediveliger, and spat), and the surrounding environment (water and algae feed) for microbial community analysis. Results We found that each larval stage has a distinct microbiome that is partially influenced by their parental microbiome, particularly the maternal egg microbiome. We also demonstrate the presence of core microbes that are consistent across all families, persist throughout early life stages (from eggs to spat), and are not detected in the microbiomes of the surrounding environment. In addition to the core microbiomes that span all life cycle stages, there is also evidence of environmentally acquired microbial communities, with earlier larval stages (D-veliger and umbo), more influenced by seawater microbiomes, and later larval stages (eyed pediveliger and spat) dominated by microbial members that are specific to oysters and not detected in the surrounding environment. Conclusion Our study characterized the succession of oyster larvae microbiomes from gametes to spat and tracked selected members that persisted across multiple life stages. Overall our findings suggest that both horizontal and vertical transmission routes are possible for the complex microbial communities associated with a broadcast spawning marine invertebrate. We demonstrate that not all members of oyster-associated microbiomes are governed by the same ecological dynamics, which is critical for determining what constitutes a hologenome.

Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

“…temperature, pH, salinity, pCO 2 ) [34][35][36][37][38]. In addition to important fluctuations in response to environmental changes, physiological status and developmental stages, the oyster microbiota shows important inter-individual variability, both at the level of the whole animal and at the level of individual tissues throughout all life stages [8, [11][12][13]39]. This heterogeneity has made it difficult to identify the core bacterial microbiota in oysters, if one exists.…”

“…As filter feeders, oysters evolve in a rich microbial environment, under constant interaction with pathogenic, commensal and beneficial microorganisms. In a recent study, Unzueta-Martínez et al showed that not all members of the oyster-associated microbiota are governed by the same ecological dynamics and that both horizontal and vertical transmission routes are possible [ 13 ]. Particularly the authors identified some members of the bacterial communities that establish at early developmental stages (from gametes to spats) and persist across multiple life stages [ 13 ].…”

“…In a recent study, Unzueta-Martínez et al showed that not all members of the oyster-associated microbiota are governed by the same ecological dynamics and that both horizontal and vertical transmission routes are possible [ 13 ]. Particularly the authors identified some members of the bacterial communities that establish at early developmental stages (from gametes to spats) and persist across multiple life stages [ 13 ]. Since initiation of the immune system occurs early in the oyster development [ 49 , 50 ], this early microbiota association raises numerous questions about its impact on the immune system maturation.…”

“…Benthic oysters not only host microbial communities on their body surfaces [ 8 ] but also in their circulating body fluids, i.e. the haemolymph (equivalent of the blood) [ 9 ], in the pallial/extrapallial cavity fluid [ 10 , 11 ] as well as in all the tissues and developmental stages studied [ 12 , 13 ]. As they are filter feeders able to concentrate microorganisms present in their environment, it has been argued that bivalves host transient microbial communities that vary with environmental conditions.…”

Maternal transmission of bacterial microbiota during embryonic development in a viviparous lizard

“…Other mechanisms include early inoculation during seed formation, egg laying, or passage through the birth canal ( 13 – 15 ). The mechanisms for vertical transmission have been extensively investigated in invertebrates, such as insects, nematodes, sponges, clams, and oysters ( 16 – 19 ). However, research on vertical transmission in vertebrates, especially other than Mammalia, has been limited.…”