Keystone molecules in the rocky intertidal: A multifunctional barnacle protein drives ecological interactions

Background/Question/Methods: Sensory systems provide critical filters that enable organisms to detect and recognize valuable resources. Trophic cascades structuring populations and communities are established to a large degree by behavioral-mediated interactions that rely on sensory inputs. Here, we identify a surface-adsorbed protein whose recognition drives ecological interactions and outcomes on rocky wave-swept shores. Using bioassay-guided fractionation followed by electrospray ionization gas-phase electrophoretic mobility molecular analysis (ESI-GEMMA), a large (~390 kDa), insoluble, novel glycoprotein (MULTIFUNCin) produced by the barnalce Balanus glandula was found to be the sensory cue underlying whelk-barnacle interactions in the upper intertidal.

Results/Conclusions: Both the mono- and dimeric forms of MULTIFUNCin evoked habitat selection and settlement of conspecific baranacle larvae, indicating the role of this glycoprotein as a seminal recruitment cue. This same protein also triggered predation by numerically dominant whelk species (Acanthinucella spirata, Nucella emarginata, N. ostrina, N. canaliculata, and N. lamellosa) on barnacle juveniles and adults in laboratory and field feeding assays using prey mimics. Complete nucleotide translation from a sequenced 5.1 kb mRNA transcript identified the glycoprotein as consisting of 1,550 amino acids (mw = 171 kDa). Structural elucidations further revealed significant homology (72%) among amino acid sequences of glycoprotein settlement cues between two barnacle species, B. glandula and Amphibalanus (Balanus) amphitrite, inhabiting different biogeographical provinces. Such homology suggests a generalizable role for this group of glycoproteins as signal molecules. As dominant competitors for space, the relative balance between barnacle recruitment and predation mortality has strong, cascading, direct and indirect effects on community dynamics. Contact protein cues, such as MULTIFUNCin, thus play essential ecological roles by acting as the sensory cues which drive the behavior that directly and indirectly structures communities in natural habitats.