Symbiont transmission in marine sponges: reproduction, development, and metamorphosis

Abstract

Marine sponges (phylum Porifera) form symbioses with diverse microbial communities that can be transmitted between generations through their developmental stages. Here, we integrate embryology and microbiology to review how symbiotic microorganisms are transmitted in this early-diverging lineage. We describe that vertical transmission is widespread but not universal, that microbes are vertically transmitted during a select developmental window, and that properties of the developmental microbiome depends on whether a species is a high or low microbial abundance sponge. Reproduction, development, and symbiosis are thus deeply rooted, but why these partnerships form remains the central and elusive tenet of these developmental symbioses.

Maternal provisioning of an obligate symbiont

“…Similar to animal hosts from diverse lineages, the bacterial community associated with sponges is a specific mix of generalists that partially form by neutral processes and a fraction of these microbes are then vertically transmitted [16, 44, 45]. This taxonomic stochasticity has led others to postulate that some maternally transmitted microbes provide little to no fitness to the sponge holobiont, of which could be depleted upon perturbation [11, 16, 46, 47]. An experimental reduction in the total bacterial community that associated with H. panicea larvae is consistent with this statement, suggesting that these other bacteria may not have an essential functional role during larval development.…”

“…Viviparity is widespread amongst animals and is particularly common in marine sponges. Brooding provides the adult sponge with a developmental window to maternally transmit microbes that are enriched within the mesohyl [11][12][13][14][15][16]. This strategy is particularly evident in low microbial abundance sponges, which inherit a select few dominant symbionts that are essential for maternal, and sometimes offspring, fitness [11,17].…”

“…Brooding provides the adult sponge with a developmental window to maternally transmit microbes that are enriched within the mesohyl [11][12][13][14][15][16]. This strategy is particularly evident in low microbial abundance sponges, which inherit a select few dominant symbionts that are essential for maternal, and sometimes offspring, fitness [11,17]. One such sponge is Halichondria panicea, a coastal species that inhabits large parts of the North Atlantic and has a bacterial community that is dominated (with a 90:1 cell count) by the obligate symbiont "Candidatus Halichondribacter symbioticus [18][19][20][21].…”

Global patterns in symbiont selection and transmission strategies in sponges

“…Animal-microbe interactions can include different levels of relationships such as mutualism, commensalism, parasitism, and pathogenic. Microbes are fundamental for the host health, nutrition, defense, reproduction and development (McFall-Ngai, 2002;Pais et al, 2008;Maldonado et al, 2012;Thomas et al, 2017;Slaby et al, 2019;Hou et al, 2022), and most of them are faithfully transmitted to the next generation to ensure that these benefits are propagated in time and perpetuated throughout generations (Chaston and Goodrich-Blair, 2010;Arora et al, 2017;Carrier et al, 2022). It is not surprising then that microbes have evolved to regulate some of the crucial steps in animal development (Nyholm, 2020), persisting as a unit of selection through generations.…”

“…Microorganisms can be incorporated to sponge eggs, sperm, embryos, and larvae (reviewed in Carrier et al, 2022), making reproduction of sponges a hot topic for microbial studies. Sponges can display all types of reproduction, from asexual to sexual reproduction, including hermaphroditism, gonochorism or successional hermaphroditism, oviparity, and viviparity.…”