Settlement and metamorphosis of planktonic larvae into benthic adults are critical components of a diverse range of marine invertebrate-mediated processes such as the formation of mussel beds and coral reefs, the recruitment of marine shellfisheries, and the initiation of macrobiofouling. Although larval settlement and metamorphosis induced by natural chemical cues is widespread among marine invertebrates, the mechanisms of action remain poorly understood. Here, we identified that the molecular target of adenosine (an inducer of larval settlement and metamorphosis from conspecific adults in the invasive biofouling mussel Mytilopsis sallei) is adenosine kinase (ADK). The results of transcriptomic analyses, pharmacological assays, temporal and spatial gene expression analyses, and siRNA interference, suggest that ATP-dependent phosphorylation of adenosine catalyzed by ADK activates the downstream AMPK-FoxO signaling pathway, inducing larval settlement and metamorphosis in M. sallei. This study not only reveals the role of the ADK-AMPK-FoxO pathway in larval settlement and metamorphosis of marine invertebrates but it also deepens our understanding of the functions and evolution of adenosine signaling, a process that is widespread in biology and important in medicine.

Summary Most marine benthic invertebrates have a pelagic larval phase, after which they settle preferentially on or near conspecific adults, forming aggregations. Although settlement pheromones from conspecific adults have been implicated as critical drivers of aggregation for more than 30 years, surprisingly few have been unambiguously identified. Here we show that in the invasive dreissenid mussel Mytilopsis sallei (an ecological and economic pest), three common purines (adenosine, inosine, and hypoxanthine) released from adults in a synergistic and precise ratio (1:1.125:3.25) serve as an aggregation pheromone by inducing conspecific larval settlement and metamorphosis. Our results demonstrate that simple common metabolites can function as species-specific pheromones when present in precise combinations. This study provides important insights into our understanding of the ecology and communication processes of invasive organisms and indicates that the combination and ratio of purines might be critical for purine-based signaling systems that are fundamental and widespread in nature.

Bacterial biofilms play an important role in marine biofouling. The formation of a biofilm starts when marine bacterial cells transition from a planktonic to an attached state. However, the molecular mechanisms involved in this transition are poorly understood. Here, 51 strains of marine bacteria were isolated from natural biofilms growing on submerged artificial surfaces (glass slides, epoxy panels, and bridge pillars) and evaluated for their biofilm-forming capacity. Eleven strains formed relatively strong biofilms and 16S rRNA gene sequence analysis indicated that they belonged to the genera Leisingera, Roseobacter, Pseudoalteromonas, Alteromonas, Tenacibaculum, Vibrio, Chryseobacterium, Aquimarina, and Acinetobacter. Strain Pseudoalteromonas sp. W-7 showed efficient and rapid attachment and was therefore chosen for further study. An iTRAQ-based comparative proteomic analysis of planktonic and attached strain W-7 cells was carried out. A total of 3468 proteins were identified, of which 163 showed significant differential expression (120 down-regulated and 43 up-regulated in attached cells relative to planktonic cells). KEGG (Kyoto encyclopedia of genes and genomes) analysis indicated that pyruvate metabolism, carbon fixation, and carbon metabolism were significantly affected in attached cells. Up-regulated proteins such as UTP-glucose-1-phosphate uridylyltransferase, acetyltransferase component of pyruvate dehydrogenase complex, OmpA-like protein, and acetyl-coenzyme A synthetase may be important during initial adhesion. Our findings provide a deeper understanding of the planktonic to sessile transition of marine fouling bacteria.

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