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The vertical transmission of microbial symbionts is a widespread phenomenon among marine sponges. Our understanding of this biological feature stems from taxonomic, geographical, and ecological biases, but, nevertheless, there is a clear spatial coordination during development (Figs. 3 and 4). For a sub-set of these sponge species, we know which symbionts serve as the inoculum for the next generation but not why they are transmitted. The assumption is that there are functional links to the biology and ecology of the dispersing larvae, but data supporting these hypotheses are currently scarce. Microbial symbionts may provide complementary resources to the developing larva once it is no longer sheltered by the adult (Fig. 3P). This may include coping with the dynamic oceanographic environment and seeking out a suitable location to settle and undergo metamorphosis. These are the focal point of the next section: to describe how the microbial communities associated with sponge larvae influence life in the plankton, how these symbiont communities are influenced by the environment, and how they may be key to transition back to the seafloor.
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Living in the water column comes with an added mortality risk. The five main sources of mortality for marine invertebrate larvae are temperature, nutritional conditions, dispersal, predation, and metamorphosis [41, 138, 139], but dysbiosis should also be considered . Sponge larvae are non-feeding (lecithotrophic) and spend only a few hours to a few days in the plankton (anchiplanic). Therefore, they are unaffected by external food availability (but not internal nutritional condition) and are less susceptible to being transported off the continental shelf. Mortality due to predation is also likely to be minimal because sponge larvae are briefly in the water column and because they appear to have chemical defenses that make them less palatable [141, 142]. Chemical defenses are symbiont-derived for larvae of the bryozoan Bugula neritina [143, 144], and this may also occur in sponges because they are a group rich in secondary metabolites with defensive roles (e.g., ). These defenses combined with a short pelagic duration may make sponges favorable for vertical transmission because the microbial cells are less likely to be wasted as a result of larval mortality.
Sponges are released as nearly competent or competent larvae that typically spend minutes to a couple weeks in the water column. Marine invertebrate larvae use a hierarchical suite of ecological signals to locate a suitable site to settle and undergo metamorphosis [50, 134, 146,147,148,149]. In the brief hiatus from the benthos, sponge larvae can face substantial local variation in temperature, salinity, and light that influence their dispersal through disruptions in development, locomotion, and behavior [149, 150]. If these ecological variables cause a prolonged larval duration and a delay in metamorphosis, then juvenile fitness will likely be compromised [136, 151]. These same ecological factors may influence animal microbiomes and, in particular, those of marine invertebrate larvae [152, 153]. Larvae from other groups of marine invertebrates horizontally acquire microbes from the seawater in response to variation in abiotic variables . It is estimated that 55% of the microbial taxa associated with sponge larvae are acquired horizontally [44, 113], but very few experiments have determined whether these horizontal acquisitions also aid in coping with environmental variation.
As marine invertebrate larvae near competency for metamorphosis, they are guided towards the seafloor by environmental cues and behavioral shifts that are not yet well-understood. Larvae of some species become denser and negatively phototactic, allowing them to sink through the water column, enter the benthic boundary layer, and explore settlement cues [50, 164]. However, this transition cannot occur without the input of specific hormones and/or other signaling compounds that may be acquired exogenously [165, 166] or from symbionts that are both vertically transmitted and metabolically active . One example of the latter is the demosponge Amphimedon queenslandica. This sponge requires nitric oxide signaling to stimulate larval settlement, but the host is unable to biosynthesize arginine [167, 168]. Instead, arginine is produced by vertically transmitted bacteria, taken up by the larval cells, and incorporated into the arginine-citrulline loop to produce nitric oxide [169,170,171]. Metabolic complementation between host and symbiont(s) is widespread [62, 172], but A. queenslandica is unique in that this principle extends to a major developmental and life cycle transition . We hypothesize that the symbiont incorporation of signaling that enables larval holobionts to undergo metamorphosis is more widespread among marine invertebrates. Such symbioses may stimulate settlement, but they can only be truly beneficial if the correct benthic substrate is found .
The most widespread settlement cue to induce metamorphosis for marine invertebrate larvae are biofilms, complex assemblages of microorganisms that coat most surfaces in the sea [173,174,175,176,177]. Larvae of some marine invertebrates (e.g., the polychaete worm Hydroides elegans) must come in contact with a specific bacterium (i.e., Pseudoalteromonas luteoviolacea) in the biofilm. In this case, P. luteoviolacea uses a contractile injection system to induce the settlement of H. elegans [174, 178,179,180]. Our present understanding is that sponge larvae locate a biofilm or conspecific cue to undergo metamorphosis [147, 173, 176]. These responses may be because sponge larvae often have a short planktonic life, and thus, being selective is less advantageous. Alternatively, specific bacterial strains on the seafloor may induce metamorphosis and involve select mechanical triggers [174, 178, 179]. These details remain unresolved in marine sponges.
Metamorphosis involves an extensive reorganization and transdifferentiation of larval cells into adult structures [181,182,183,184,185]. This transition takes hours to days and can be accompanied by a major reconstruction in the associated bacterial community [117, 169]. For example, Carteriospongia foliascens has a stable bacterial community throughout this transition, while that of A. queenslandica changes drastically due to an influx of environmentally derived bacteria [160, 169]. These associations are short-lived for A. queenslandica. Juveniles upregulate genes involved in innate immunity (e.g., scavenger receptors) and host-microbe crosstalk (e.g., ankyrins) that allow for the vertically inherited symbionts to replace these environmental bacteria as the sponge reaches adulthood . The shift away from resident members of the symbiont community would appear to be maladaptive and this interpretation may simply be due to our limited understand of metamorphosis in sponges.
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In this Review, we have described the general patterns of symbiont transmission in marine sponges during reproduction, development, and metamorphosis. Here, we highlight 5 key points from this Review:
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Close view of phosphoprotein spots (spots 1-11) differentially expressed (indicated by arrows) during metamorphosis in P. vexillosa. (A): Enlarged phosphoprotein gels (Pre: pre-competent larvae, Com: competent larvae, Juv: juveniles). (B) Relative intensity of the differentially regulated phosphoproteins. (C) Phosphoprotein-to protein intensity ratios.
Close view of phosphoprotein spots (spots 12-21) differentially expressed (indicated by arrows) during metamorphosis in P. vexillosa. (A) Enlarged phosphoprotein gels (Pre: pre-competent larvae, Com: competent larvae, Juv: juveniles). (B) Relative intensity of the differentially regulated phosphoproteins. (C) Phosphoprotein-to-protein intensity ratios.
Close view of phosphoprotein spots (spots 22-32) differentially expressed (indicated by arrows) during metamorphosis in P. vexillosa. (A) Enlarged phosphoprotein gels (Pre: pre-competent larvae, Com: competent larvae, Juv: juveniles). (B) Relative intensity of the differentially regulated phosphoproteins. (C) Phosphoprotein-to-protein intensity ratios.
2-DE Western blot analysis during metamorphosis in P. vexillosa. Two-dimensional gel and immunoblot of tubulin (A) and actin (B) of P.vexillosa (Precom: pre-competent larvae, Com: competent larvae, Juv: juveniles) probed with anti-tubulin and anti-actin monoclonal antibodies and developed by ECL western blotting analysis system.
MHC is also used as a marker of the physiological and developmental states of muscle , and it can be involved in the degeneration of the caudal muscle by apoptosis , the formation of new muscle (secondary myogenesis) , and the conversion of larval muscles to adult muscles . The up-regulation of MHC in COM larvae and its subsequent down-regulation during metamorphosis may suggest the presence of a large proportion of larval myofibers that subsequently disappear during the processes of attaining competency and metamorphosis. Large amounts of myofibrillar proteins need to be synthesized to build up the muscles during metamorphosis.