Larval settlement and metamorphosis in a marine gastropod in response to multiple conspecific cues.
Ontology highlight
ABSTRACT:
SUBMITTER: Cahill AE
PROVIDER: S-EPMC4974925 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:As a stage of life cycle, larval settlement and metamorphosis are critical processes for persistence of many marine invertebrate populations. Bacterial biofilms (BFs) could induce larval settlement and metamorphosis. Pseudoalteromonas, a widely distributed genus of marine bacteria, showed inductive effects on several invertebrates. However, how Pseudoalteromonas BFs induce settlement and metamorphosis of Mytilus coruscus remains unclear. Pseudoalteromonas marina BFs with the highest inducing activity were further investigated to define inductive cues. Surface-bound products of P. marina BFs could induce larval settlement and metamorphosis. P. marina BFs treated with formalin, antibiotics, ultraviolet irradiation, heat and ethanol significantly reduced inductive effects and cell survival rates. The confocal laser scanning microscopy and the biovolume analysis showed the dominance of α-polysaccharides on P. marina BFs. Treatment of BFs with amylases, proteases and lipase led to the decrease of inducing activity, suggesting that inductive cues of P. marina BFs may comprise of molecular domains of polysaccharides, proteins, and lipids. Finding inductive cues of BFs could put forward further studies about the mechanism of larval settlement and metamorphosis of marine invertebrates.
| S-EPMC7018757 | biostudies-literature
Project description:Biofilms are critical components of most marine systems and provide biochemical cues that can significantly impact overall community composition. Although progress has been made in the bacteria-animal interaction, the molecular basis of modulation of settlement and metamorphosis in most marine animals by bacteria is poorly understood. Here, Pseudoalteromonasmarina showing inducing activity on mussel settlement and metamorphosis was chosen as a model to clarify the mechanism that regulates the bacteria-mussel interaction. We constructed a flagellin synthetic protein gene fliP deletion mutant of P. marina and checked whether deficiency of fliP gene will impact inducing activity, motility, and extracellular polymeric substances of biofilms. Furthermore, we examined the effect of flagellar proteins extracted from bacteria on larval settlement and metamorphosis. The deletion of the fliP gene caused the loss of the flagella structure and motility of the ∆fliP strain. Deficiency of the fliP gene promoted the biofilm formation and changed biofilm matrix by reducing β-polysaccharides and increasing extracellular proteins and finally reduced biofilm-inducing activities. Flagellar protein extract promoted mussel metamorphosis, and ∆fliP biofilms combined with additional flagellar proteins induced similar settlement and metamorphosis rate compared to that of the wild-type strain. These findings provide novel insight on the molecular interactions between bacteria and mussels.
| S-EPMC7036800 | biostudies-literature
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.
| S-EPMC6677853 | biostudies-literature
Project description:Marine pelagic larvae from throughout the animal kingdom use a hierarchy of environmental cues to identify a suitable benthic habitat on which to settle and metamorphose into the reproductive phase of the life cycle. The majority of larvae are induced to settle by biochemical cues and many species have long been known to preferentially settle in the dark. Combined, these data suggest that larval responses to light and biochemical cues may be linked, but this is yet to be explored at the molecular level. Here, we track vertical position of larvae of the sponge Amphimedon queenslandica to show that they descend to the benthos at twilight, by which time they are competent to respond to biochemical cues, consistent with them naturally settling in the dark. We then conduct larval settlement assays under three different light regimes (natural day-night, constant dark or constant light), and use transcriptomics on individual larvae to identify candidate molecular pathways underlying the different settlement responses that we observe. We find that constant light prevents larval settlement in response to biochemical cues, likely via actively repressing chemostransduction; this is consistent with the sustained upregulation of a photosensory cryptochrome and two putative inactivators of G-protein signalling in the constant light only. We hypothesise that photo- and chemosensory systems may be hierarchically integrated into ontogeny to regulate larval settlement via nitric oxide (NO) and cyclic guanosine monophosphate (cGMP) signalling in this sponge that belongs to one of the earliest branching of the extant animal lineages.
2019-10-09 | GSE130274 | GEO
Project description:Microbial biofilms play important roles in initiating settlement of marine invertebrate larvae. Given the importance of habitat selection by the motile larval phase, understanding settlement choices is critical if we are to successfully predict the population dynamics of sessile adults. Marine microbial biofilms show remarkable variability in community composition, often mediated by environmental conditions and biofilm age. To determine if biofilm communities were influenced by the time allowed to establish (age) and/or seawater temperature, we manipulated experimental surfaces to firstly determine biofilm community composition and secondly test larval settlement responses for the abundant coral reef sponge Rhopaloeides odorabile. Microbial profiling of biofilms revealed different communities according to both age and temperature. Biofilm community composition, as a result of both elevated seawater temperature and biofilm age, contributed to settlement for sponge larvae with markedly higher numbers of larvae settling to biofilms developed over longer periods (10 d) and at temperatures 2-6°C above ambient.
| S-EPMC3921630 | biostudies-other
Project description: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.
| S-EPMC8118285 | biostudies-literature
Project description:Ocean acidification (OA) increasingly threatens marine systems, and is especially harmful to calcifying organisms. One important question is whether OA will alter species interactions. Crustose coralline algae (CCA) provide space and chemical cues for larval settlement. CCA have shown strongly negative responses to OA in previous studies, including disruption of settlement cues to corals. In California, CCA provide cues for seven species of harvested, threatened, and endangered abalone. We exposed four common CCA genera and a crustose calcifying red algae, Peyssonnelia (collectively CCRA) from California to three pCO2 levels ranging from 419-2,013 µatm for four months. We then evaluated abalone (Haliotis rufescens) settlement under ambient conditions among the CCRA and non-algal controls that had been previously exposed to the pCO2 treatments. Abalone settlement and metamorphosis increased from 11% in the absence of CCRA to 45-69% when CCRA were present, with minor variation among CCRA genera. Though all CCRA genera reduced growth during exposure to increased pCO2, abalone settlement was unaffected by prior CCRA exposure to increased pCO2. Thus, we find no impacts of OA exposure history on CCRA provision of settlement cues. Additionally, there appears to be functional redundancy in genera of CCRA providing cues to abalone, which may further buffer OA effects.
| S-EPMC5515930 | biostudies-literature
Project description:Bacteria are important mediators of the larval transition from pelagic to benthic environments for marine organisms. Bacteria can therefore dictate species distribution and success of an individual. Despite the importance of marine bacteria to animal ecology, the identity of inductive microbes for many invertebrates are unknown. Here, we report the first successful isolation of bacteria from natural substrates capable of inducing settlement and metamorphosis of the planula larvae stage of a true jellyfish, the upside-down jellyfish Cassiopea xamachana. Inductive bacteria belonged to multiple phyla, with various capacity to induce settlement and metamorphosis. The most inductive isolates belonged to the genus Pseudoalteromonas, a marine bacterium known to induce the pelago-benthic transition in other marine invertebrates. In sequencing the genome of the isolated Pseudoalteromonas and a semiinductive Vibrio, we found biosynthetic pathways previously implicated in larval settlement were absent in Cassiopea inducing taxa. We instead identified other candidate biosynthetic gene clusters involved in larval metamorphosis. These findings could provide hints to the ecological success of C. xamachana compared to sympatric congeneric species within mangrove environments and provide avenues to investigate the evolution of animal-microbe interactions. IMPORTANCE The pelagic to benthic transition for the larvae of many marine invertebrate species are thought to be triggered by microbial cues. The microbial species and exact cue that initiates this transition remains unknown for many animals. Here, we identify two bacterial species, a Pseudoalteromonas and a Vibrio, isolated from natural substrate that induce settlement and metamorphosis of the upside-down jellyfish Cassiopea xamachana. Genomic sequencing revealed both isolates lacked genes known to induce the life history transition in other marine invertebrates. Instead, we identified other gene clusters that may be important for jellyfish settlement and metamorphosis. This study is the first step to identifying the bacterial cue for C. xamachana, an ecologically important species to coastal ecosystems and an emerging model system. Understanding the bacterial cues provides insight into marine invertebrate ecology and evolution of animal-microbe interactions.
| S-EPMC10286705 | biostudies-literature
Project description:The morphogenetic transition of motile coral larvae into sessile primary polyps is triggered and genetically programmed upon exposure to environmental biomaterials, such as crustose coralline algae (CCA) and bacterial biofilms. Although the specific chemical cues that trigger coral larval morphogenesis are poorly understood there is much more information available on the genes that play a role in this early life phase. Putative chemical cues from natural biomaterials yielded defined chemical samples that triggered different morphogenetic outcomes: an extract derived from a CCA-associated Pseudoalteromonas bacterium that induced metamorphosis, characterized by non-attached metamorphosed juveniles; and two fractions of the CCA Hydrolithon onkodes (Heydrich) that induced settlement, characterized by attached metamorphosed juveniles. In an effort to distinguish the genes involved in these two morphogenetic transitions, competent larvae of the coral Acropora millepora were exposed to these predictable cues and the expression profiles of 47 coral genes of interest (GOI) were investigated after only 1 hour of exposure using multiplex RT-qPCR. Thirty-two GOI were differentially expressed, indicating a putative role during the early regulation of morphogenesis. The most striking differences were observed for immunity-related genes, hypothesized to be involved in cell recognition and adhesion, and for fluorescent protein genes. Principal component analysis of gene expression profiles resulted in separation between the different morphogenetic cues and exposure times, and not only identified those genes involved in the early response but also those which influenced downstream biological changes leading to larval metamorphosis or settlement.
| S-EPMC3954620 | biostudies-other
Project description:Bacterial outer membrane vesicles (OMVs) contain a variety of chemical compounds and play significant roles in maintaining symbiotic relationships in a changing ocean, but little is known about their function, particularly in sponge larval development. During the growth of sponge Tedania sp., OMVs from Bacteroidetes species significantly promoted larval settlement, and Tenacibaculum mesophilum SP-7-OMVs were selected as a representative strain for further investigation. According to OMVs metabolomics, larval settlement might be connected to organic acids and derivatives. The multiomics analysis of the T. mesophilum genome, SP-7-OMVs metabolome, and larval transcriptome revealed 47 shared KEGG pathways. Among the number of candidate metabolites, arginine was chosen for its greater ability to increase the settlement rate and its role as the principal substrate for nitric oxide (NO) synthesis of sponge larvae. In summary, these results demonstrated that sponge-associated bacteria might utilize OMVs and their cargo to support host development and make up for host metabolic pathway deficiencies. This study enhances our fundamental knowledge of OMVs in interactions between metazoan hosts and microorganisms that are crucial in the coevolution of marine ecosystems and the complex marine environment.
| S-EPMC10925772 | biostudies-literature