Not That Close to Mommy: Horizontal Transmission Seeds the Microbiome Associated with the Marine Sponge Plakina cyanorosea

Abstract

Marine sponges are excellent examples of invertebrate–microbe symbioses. In this holobiont, the partnership has elegantly evolved by either transmitting key microbial associates through the host germline and/or capturing microorganisms from the surrounding seawater. We report here on the prokaryotic microbiota during different developmental stages of Plakina cyanorosea and their surrounding environmental samples by a 16S rRNA metabarcoding approach. In comparison with their source adults, larvae housed slightly richer and more diverse microbial communities, which are structurally more related to the environmental microbiota. In addition to the thaumarchaeal Nitrosopumilus, parental sponges were broadly dominated by Alpha- and Gamma-proteobacteria, while the offspring were particularly enriched in the Vibrionales, Alteromonodales, Enterobacterales orders and the Clostridia and Bacteroidia classes. An enterobacterial operational taxonomic unit (OTU) was the dominant member of the strict core microbiota. The most abundant and unique OTUs were not significantly enriched amongst the microbiomes from host specimens included in the sponge microbiome project. In a wider context, Oscarella and Plakina are the sponge genera with higher divergence in their associated microbiota compared to their Homoscleromorpha counterparts. Our results indicate that P. cyanorosea is a low microbial abundance sponge (LMA), which appears to heavily depend on the horizontal transmission of its microbial partners that likely help the sponge host in the adaptation to its habitat.

Contribution of Maternal and Paternal Transmission to Bacterial Colonization in Nematostella vectensis

“…Thereby, vertically transmitted bacteria may represent beneficial symbionts, necessary for animals’ development and physiology, bacteria that lack a free-living stage, or more simply, bacteria that are present in the open water in too low abundance to be recruited ( Salerno et al, 2005 ; Bright and Bulgheresi, 2010 ). So far, few studies have undertaken a detailed comparison of microbial communities of parents, gametes and progeny in marine organisms ( Sipe et al, 2000 ; Bright and Bulgheresi, 2010 ; Sharp et al, 2012 ; Leite et al, 2017 ; Quigley et al, 2017 , 2018 , 2019 ; Bernasconi et al, 2019 ; Damjanovic et al, 2020a ; Oliveira et al, 2020 ; Igawa-Ueda et al, 2021 ).…”

“…An accredited idea among authors was that species that brood their larvae, transmit symbionts to the next generations through direct contact of the parents with the offspring ( Bright and Bulgheresi, 2010 ; Di Camillo et al, 2012 ; Bernasconi et al, 2019 ), while transmission in broadcast spawners, is dominated by horizontal transfer of bacteria from the surrounding water ( van Oppen and Blackall, 2019 ). As more studies are being conducted, there are more evidences that do not necessarily support this idea ( Nussbaumer et al, 2006 ; Apprill et al, 2012 ; Leite et al, 2017 ; Björk et al, 2019 ; Oliveira et al, 2020 ). Many broadcast spawners pass their symbionts to their offspring by incorporating them into the mucus that envelops oocyte and sperm bundles ( Ceh et al, 2012 ; Ricardo et al, 2016 ; Leite et al, 2017 ) and a wide spectrum of mixed-mode transmission in brooders and in free and broadcast spawners is revealed ( Sipkema et al, 2015 ; Fieth et al, 2016 ; Bernasconi et al, 2019 ; Damjanovic et al, 2020b ).…”

Global patterns in symbiont selection and transmission strategies in sponges

“…In support, many obligate insect-microbe interactions, such as those described between Buchneraaphid (Buchner, 1965), Wolbachia-nematode (Mclaren et al, 1975), and Ishikawaella-stinkbug (Fukatsu and Hosokawa, 2002) are transmitted from parents to offspring. However, many organisms, do not pass on their symbionts vertically (Oliveira et al, 2020b). Prominent examples of essential microbes exclusively acquired via horizontal transmission include the bioluminescent Vibrio fischeri in bobtail squids (McFall-Ngai, 2014), the nitrogen-fixing rhizobia in legumes (Simms and Taylor, 2002;Remigi et al, 2016), the hydrothermal vent tubeworm Riftia pachyptila and its Endoriftia persephone symbiont (Dubilier et al, 2001;Robidart et al, 2008), and water fleas Daphnia magna (Mushegian and Ebert, 2017).…”

“…The importance of HA in shaping the microbiome is progressively taking a more relevant role. It is becoming clearer, that essential sponge symbionts can be found in sea water, albeit in low abundances (considered the seed bank) (Webster et al, 2010), and they are major contributors to the sponge 10.3389/fevo.2022.1015592 microbiome (Turon et al, 2018;Wu et al, 2018;Sacristán-Soriano et al, 2019;Oliveira et al, 2020b). Turon et al (2018) calculated that half of the sponge species studied shared >50% relative abundance of the core microbiome with the seawater microbial core.…”

“…Sampling the microbiome from oocytes and embryos is difficult due to the challenge of isolating these elements from the adult of most species, and there has been more focus on the easier-to-sample larval stage. Research has shown that the microbiome of sponge larvae, although somewhat similar to the mother sponge, is usually a subset of the diversity hosted in the adult, that can show more or less similarity depending on the species (Steger et al, 2008;Webster et al, 2010;Fieth et al, 2016;Wu et al, 2018;Sacristán-Soriano et al, 2019;Luter et al, 2020;Oliveira et al, 2020b). However, many studies pooled several reproductive elements together and this could homogenize the sampled community, making it more similar to the mother sponge and masking individual variability.…”