It's a Small World After All: The Remarkable but Overlooked Diversity of Venomous Organisms, with Candidates Among Plants, Fungi, Protists, Bacteria, and Viruses.

Abstract

Numerous organisms, including animals, plants, fungi, protists, and bacteria, rely on toxins to meet their needs. Biological toxins have been classified into three groups: poisons transferred passively without a delivery mechanism; toxungens delivered to the body surface without an accompanying wound; and venoms conveyed to internal tissues via the creation of a wound. The distinctions highlight the evolutionary pathways by which toxins acquire specialized functions. Heretofore, the term venom has been largely restricted to animals. However, careful consideration reveals a surprising diversity of organisms that deploy toxic secretions via strategies remarkably analogous to those of venomous animals. Numerous plants inject toxins and pathogenic microorganisms into animals through stinging trichomes, thorns, spines, prickles, raphides, and silica needles. Some plants protect themselves via ants as venomous symbionts. Certain fungi deliver toxins via hyphae into infected hosts for nutritional and/or defensive purposes. Fungi can possess penetration structures, sometimes independent of the hyphae, that create a wound to facilitate toxin delivery. Some protists discharge harpoon-like extrusomes (toxicysts and nematocysts) that penetrate their prey and deliver toxins. Many bacteria possess secretion systems or contractile injection systems that can introduce toxins into targets via wounds. Viruses, though not "true" organisms according to many, include a group (the bacteriophages) which can inject nucleic acids and virion proteins into host cells that inflict damage rivaling that of conventional venoms. Collectively, these examples suggest that venom delivery systems-and even toxungen delivery systems, which we briefly address-are much more widespread than previously recognized. Thus, our understanding of venom as an evolutionary novelty has focused on only a small proportion of venomous organisms. With regard to this widespread form of toxin deployment, the words of the Sherman Brothers in Disney's iconic tune, It's a Small World, could hardly be more apt: "There's so much that we share, that it's time we're aware, it's a small world after all".