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The natural sequence of events in larval settlement and metamorphosis of Hydroides elegans (Polychaeta; Serpulidae).

ABSTRACT: The broadly distributed serpulid worm Hydroides elegans has become a model organism for studies of marine biofouling, development and the processes of larval settlement and metamorphosis induced by surface microbial films. Contrasting descriptions of the initial events of these recruitment processes, whether settlement is induced by (1) natural multi-species biofilms, (2) biofilms composed of single bacterial species known to induce settlement, or (3) a bacterial extract stimulated the research described here. We found that settlement induced by natural biofilms or biofilms formed by the bacterium Pseudoalteromonas luteoviolacea is invariably initiated by attachment and secretion of an adherent and larva-enveloping primary tube, followed by loss of motile cilia and ciliated cells and morphogenesis. The bacterial extract containing complex tailocin arrays derived from an assemblage of phage genes incorporated into the bacterial genome appears to induce settlement events by destruction of larval cilia and ciliated cells, followed by attachment and primary-tube formation. Similar destruction occurred when precompetent larvae of H. elegans or larvae of a nudibranch gastropod were exposed to the extract, although neither of them metamorphosed. We argue that larvae that lose their cilia before attachment would be swept away from the sites that stimulated settlement by the turbulent flow characteristic of most marine habitats.

SUBMITTER: Hadfield MG

PROVIDER: S-EPMC8118285 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Marine bacterial biofilms have long been recognized as potential inducers of larval settlement and metamorphosis in marine invertebrates, but few chemical cues from bacteria have been identified. Here, we show that larval settlement and metamorphosis of an invasive fouling mussel, Mytilopsis sallei, could be induced by biofilms of bacteria isolated from its adult shells and other substrates from the natural environment. One of the strains isolated, Vibrio owensii MS-9, showed strong inducing activity which was attributed to the release of a mixture of nucleobases including uracil, thymine, xanthine, hypoxanthine, and guanine into seawater. In particular, the synergistic effect of hypoxanthine and guanine was sufficient for the inducing activity of V. owensii MS-9. The presence of two or three other nucleobases could enhance, to some extent, the activity of the mixture of hypoxanthine and guanine. Furthermore, we determined that bacteria producing higher concentrations of nucleobases were more likely to induce larval settlement and metamorphosis of M. sallei than were bacteria producing lower concentrations of nucleobases. The present study demonstrates that bacterial nucleobases play an important role in larval settlement and metamorphosis of marine invertebrates. This provides new insights into our understanding of the role of environmental bacteria in the colonization and aggregation of invasive fouling organisms and of the metabolites used as chemical mediators in cross-kingdom communication within aquatic systems.IMPORTANCE Invasive species are an increasingly serious problem globally. In aquatic ecosystems, invasive dreissenid mussels are well-known ecological and economic pests because they appear to effortlessly invade new environments and foul submerged structures with high-density aggregations. To efficiently control exotic mussel recruitment and colonization, the need to investigate the mechanisms of substrate selection for larval settlement and metamorphosis is apparent. Our work is one of very few to experimentally demonstrate that compounds produced by environmental bacteria play an important role in larval settlement and metamorphosis in marine invertebrates. Additionally, this study demonstrates that bacterial nucleobases can be used as chemical mediators in cross-kingdom communication within aquatic systems, which will enhance our understanding of how microbes induce larval settlement and metamorphosis of dreissenid mussels, and it furthermore may allow the development of new methods for application in antifouling.

Project description:As a service to taxonomists and ecologists using names in the well-known and species-rich ship-fouling serpulid genus Hydroides we present an update of all 107 non-synonymised scientific names, with additional information on Hydroides nomenclature, original names, etymologies, and type localities derived from original literature, and in accord with the World Register of Marine Species (WoRMS) database. An update is needed because the gender of genus Hydroides has from 1 January 2000 reverted to the original feminine, due to a change in the wording of International Code of Zoological Nomenclature which was overlooked at that time, and is contrary to the usage in practice of Hydroides as masculine which had started about 1992, although Code-required from the 1960s. We match 31 further original names of current WoRMS subjective junior synonyms to each non-synonymised name, and also report on the world distribution of the genus as illustrated by type localities of the valid names. We include notes on seven species inquirenda. The correct rendering is given of six names that have been altered for gender agreement for the first time herein. Hydroides gottfriedinom. n. replaces junior homonym Hydroides rostrata Pillai, 1971. Currently there are 41 non-synonymised species-group names in Hydroides which should be gender invariant, and 23 names which would only change if moved to a neuter genus; the remaining 43 names are fully gender variable. Place-names (23), and personal names (16) make up more than a third (36%) of the species names, with most of the remainder (68) being descriptive of species character states, usually of operculum morphology (54). All species, except Hydroides norvegica (63°N), have type localities in shallow-water coastal locations in temperate to tropical waters below latitude 44°, with the highest number of new species (54) from the adjoining Western Pacific and Indian Ocean areas. The other concentration of new species (31) are those first found on the Pacific and Atlantic coasts of North America and in the Caribbean.

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The natural sequence of events in larval settlement and metamorphosis of Hydroides elegans (Polychaeta; Serpulidae).

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