title: Keystone predation and molecules of keystone significance.
abstract: Keystone species structure ecological communities and are major determinants of biodiversity. A synthesis of research on keystone species is nonetheless missing a critical component - the sensory mechanisms for behavioral interactions that determine population- and community-wide attributes. Here, we establish the chemosensory basis for keystone predation by sea stars (Pisaster ochraceus) on mussels. This consumer-resource interaction is prototypic of top-down driven trophic cascades. Each mussel species (Mytilus californianus and M. galloprovincialis) secretes a glycoprotein orthologue (29.6 and 28.1 kDa, respectively) that acts, singularly, to evoke the sea star predatory response. The orthologues (named "KEYSTONEin") are localized in the epidermis, extrapallial fluid, and organic shell coating (periostracum) of live, intact mussels. Thus, KEYSTONEin contacts chemosensory receptors on tube feet as sea stars crawl over rocky surfaces in search of prey. The complete nucleotide sequences reveal that KEYSTONEin shares 87% (M. californianus) or 98% (M. galloprovincialis) homology with a calcium-binding protein in the shell matrix of a closely related congener, M. edulis. All three molecules cluster tightly within the Complement Component 1 Domain Containing (C1qDC) protein family; each exhibits a large globular domain, low complexity region(s), coiled coil, and at least four of five histidine-aspartic acid tandem motifs. Collective results support the hypothesis that KEYSTONEin evolved ancestrally in immunological, and later, in biomineralization roles. More recently, the substance has become exploited by sea stars as a contact cue for prey recognition. As the first identified compound to evoke keystone predation, KEYSTONEin provides valuable sensory information, promotes biodiversity, and shapes community structure and function. Without this molecule, there would be no predation by sea stars on mussels.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095, USA.|Moreton Bay Research Station, Centre for Marine Science, School of Biological Sciences, University of Queensland, Brisbane, Queensland, 4072, Australia.
authors.forename: Richard K
authors.initials: RK
authors.lastname: Zimmer
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095, USA.
authors.forename: Graham A
authors.initials: GA
authors.lastname: Ferrier
authors.affiliation: Department of Chemistry and Biochemistry, University of California, Los Angeles, California, 90095, USA.
authors.forename: Steven J
authors.initials: SJ
authors.lastname: Kim
authors.affiliation: Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, California, 90095, USA.|UCLA/DOE Institute for Genomics and Proteomics, University of California, Los Angeles, California, 90095, USA.
authors.forename: Rachel R
authors.initials: RR
authors.lastname: Ogorzalek Loo
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California, 90095, USA.|Moreton Bay Research Station, Centre for Marine Science, School of Biological Sciences, University of Queensland, Brisbane, Queensland, 4072, Australia.
authors.forename: Cheryl Ann
authors.initials: CA
authors.lastname: Zimmer
authors.affiliation: Department of Chemistry and Biochemistry, University of California, Los Angeles, California, 90095, USA.|Department of Biological Chemistry, David Geffen School of Medicine, University of California, Los Angeles, California, 90095, USA.|UCLA/DOE Institute for Genomics and Proteomics, University of California, Los Angeles, California, 90095, USA.
authors.forename: Joseph A
authors.initials: JA
authors.lastname: Loo
mesh_terms: D000818:Animals; D044822:Biodiversity; D017753:Ecosystem; D049878:Mytilus; D011235:Predatory Behavior; D013215:Starfish
keywords: Mytilus californianus; Mytilus galloprovincialis; Pisaster ochraceus; chemical cue; community ecology; foundation species; glycoprotein; intertidal ecology; keystone predation; mussel; sea star; sensory ecology