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.

Chemical cues for intraspecific chemical communication and interspecific interactions in aquatic environments: applications for fisheries and aquaculture

“…30 kDa and approx. 200 kDa and its dimer) to find specific prey (Ferrier et al 2016;Zimmer et al 2017), and protein complexes to achieve gregarious settlement (Matsumura et al 1998;Dreanno et al 2007). A wide range of molecules, including sugars (Jager 1970;Weissburg and Zimmer-Faust 1991), amino acids (Yambe et al 2006a), nucleotides (Zimmer-Faust 1993), pyrimidine bases and nucleosides (Kicklighter et al 2007), lipids (Sakata et al 1988), and steroids (Dulka et al 1987), can be chemical stimuli.…”

“…Since chemical compounds affect the behavior of other organisms, some organisms emit defensive compounds to deter and/or deceive predators and parasites. Studies on these chemically mediated interactions among organisms provide insights into the ecology and evolution of marine communities (Hay 2009;Zimmer et al 2017).…”

Chemosensory Exploitation and Predator-Prey Arms Races

“…A different organic enrichment control (BSA) therefore was needed. We used bovine serum albumin to be consistent with our previous studies (Zimmer et al, 2016b(Zimmer et al, , 2017.…”

Low abundance members of the gut microbiome are potent drivers of immune cell education

“…Experimental manipulations such as removing putative keystone members to assess their impact are used routinely by ecologist studying plants and animal communities (15,16).…”