Global patterns in symbiont selection and transmission strategies in sponges

Abstract

Sponges host dense and diverse communities of microbes (known as the microbiome) beneficial for the host nutrition and defense. Symbionts in turn receive shelter and metabolites from the sponge host, making their relationship beneficial for both partners. Given that sponge-microbes associations are fundamental for the survival of both, especially the sponge, such relationship is maintained through their life and even passed on to the future generations. In many organisms, the microbiome has profound effects on the development of the host, but the influence of the microbiome on the reproductive and developmental pathways of the sponges are less understood. In sponges, microbes are passed on to oocytes, sperm, embryos, and larvae (known as vertical transmission), using a variety of methods that include direct uptake from the mesohyl through phagocytosis by oocytes to indirect transmission to the oocyte by nurse cells. Such microbes can remain in the reproductive elements untouched, for transfer to offspring, or can be digested to make the yolky nutrient reserves of oocytes and larvae. When and how those decisions are made are fundamentally unanswered questions in sponge reproduction. Here we review the diversity of vertical transmission modes existent in the entire phylum Porifera through detailed imaging using electron microscopy, available metabarcoding data from reproductive elements, and macroevolutionary patterns associated to phylogenetic constraints. Additionally, we examine the fidelity of this vertical transmission and possible reasons for the observed variability in some developmental stages. Our current understanding in marine sponges, however, is that the adult microbial community is established by a combination of both vertical and horizontal (acquisition from the surrounding environment in each new generation) transmission processes, although the extent in which each mode shapes the adult microbiome still remains to be determined. We also assessed the fundamental role of filtration, the cellular structures for acquiring external microbes, and the role of the host immune system, that ultimately shapes the stable communities of prokaryotes observed in adult sponges.

Maternal provisioning of an obligate symbiont in a sponge

“…The vertical transmission of maternal microbes is ancient, evolutionarily advantageous, and occurs for single mutualists as well as diverse prokaryotic communities (Bright & Bulgheresi, 2010 ; Carrier & Bosch, 2022 ; Funkhouser & Bordenstein, 2013 ; McFall‐Ngai, 2002 ; Moran & Wernegreen, 2000 ). Most major metazoan lineages have been observed to transmit microbes from mother to offspring [annelids (Davidson & Stahl, 2008 ), arthropods (Ferree et al, 2005 ), chordates (Hirose, 2015 ), cnidarians (Apprill et al, 2009 ), echinoderms (Carrier et al, 2021 ), flatworms (Jäckle et al, 2019 ), molluscs (Cary & Giovannoni, 1993 ), nematodes (Stevens et al, 2001 ), and sponges (Carrier et al, 2022 ; Díez‐Vives et al, 2022 )]. These developmental symbionts have deep evolutionary origins and play integral roles in host biology and ecology, including acclimation (Foutaine et al, 2022 ), gametogenesis (Dedeine et al, 2001 ), and metamorphosis (Song et al, 2021 ).…”

“…In this, fertilization occurs internally, early embryos are brooded within the maternal body, and late‐stage offspring are released into the environment. Viviparity is widespread among animals and is particularly common in marine sponges (Díez‐Vives et al, 2022 ). Brooding provides the adult sponge with a developmental window to transmit maternal microbes that are within the mesohyl (Björk et al, 2019 ; Carrier et al, 2022 ; Díez‐Vives et al, 2022 ; Maldonado, 2007 ; Maldonado & Riesgo, 2009 ; Riesgo et al, 2007 ).…”

“…Viviparity is widespread among animals and is particularly common in marine sponges (Díez‐Vives et al, 2022 ). Brooding provides the adult sponge with a developmental window to transmit maternal microbes that are within the mesohyl (Björk et al, 2019 ; Carrier et al, 2022 ; Díez‐Vives et al, 2022 ; Maldonado, 2007 ; Maldonado & Riesgo, 2009 ; Riesgo et al, 2007 ). This is particularly evident in ‘low microbial abundance’ sponges, which inherit a select few dominant symbionts that are essential for maternal fitness (Carrier et al, 2022 ; Song et al, 2021 ).…”

“…Most major metazoan lineages have been observed to transmit microbes from mother to offspring [annelids (Davidson & Stahl, 2008), arthropods (Ferree et al, 2005), chordates (Hirose, 2015), cnidarians (Apprill et al, 2009), echinoderms (Carrier et al, 2021), flatworms (Jäckle et al, 2019), molluscs (Cary & Giovannoni, 1993), nematodes (Stevens et al, 2001), and sponges Díez-Vives et al, 2022)]. These developmental symbionts have deep evolutionary origins and play integral roles in host biology and ecology, including acclimation (Foutaine et al, 2022), gametogenesis (Dedeine et al, 2001), and metamorphosis (Song et al, 2021).…”

Novel nitrifying symbiont lineages are vertically inherited and widespread in marine sponges

“…Their evolutionary and ecological success can partly be attributed to the diverse metabolic interactions with the abundant microbiome members they harbour in their tissue (6)(7)(8). Despite their ability to filter large amounts of seawater resulting in constant exposure to environmental microbes (9,10), sponges discriminate between symbionts and food extremely well (11).…”