Glowing Worms: Biological, Chemical, and Functional Diversity of Bioluminescent Annelids

Integrative and Comparative Biology Integrative and Comparative Biology, volume 57, number 1, pp. 18–32 doi:10.1093/icb/icx017 Society for Integrative and Comparative Biology INVITED REVIEW Glowing Worms: Biological, Chemical, and Functional Diversity of Bioluminescent Annelids Aida Verdes1,*,†,‡ and David F. Gruber1,*,† 1 E-mail: ; Abstract Bioluminescence, the ability to produce light by living organisms, has evolved independently in numerous lineages across the tree of life. Luminous forms are found in a wide range of taxonomic groups from bacteria to vertebrates, although the great majority of bioluminescent organisms are marine taxa. Within the phylum Annelida, bioluminescence is widespread, present in at least 98 terrestrial and marine species that represent 45 genera distributed in thirteen lineages of clitellates and polychaetes. The ecological diversity of luminous annelids is unparalleled, with species occupying a great variety of habitats including both terrestrial and marine ecosystems, from coastal waters to the deepsea, in benthic and pelagic habitats from polar to tropical regions. This great taxonomic and ecological diversity is matched by the wide array of bioluminescent colors—including yellow light, which is very rare among marine taxa— different emission wavelengths even between species of the same genus, and varying patterns, chemical reactions and kinetics. This diversity of bioluminescence colors and patterns suggests that light production in annelids might be involved in a variety of different functions, including defensive mechanisms like sacrificial lures or aposematic signals, and intraspecific communication systems. In this review, we explore the world of luminous annelids, particularly focusing on the current knowledge regarding their taxonomic and ecological diversity and discussing the putative functions and chemistries of their bioluminescent systems. Introduction The phylum Annelida, more commonly known as segmented or bristle worms, is an ancient and ecologically important lineage of Lophotrochozoans, with around 17,000 described species (Struck et al. 2011; Weigert and Bleidorn 2016). Annelids are present in a wide variety of environments ranging from terrestrial and freshwater to marine habitats, including species that are highly specialized to occupy unique ecological niches such as hydrothermal vents or whale falls (Rouse and Pleijel 2001; Struck et al. 2011; Purschke et al. 2014; Weigert and Bleidorn 2016). Subsequent adaptive radiations within Annelida have led to the remarkably high species diversity we see today and have also resulted in an extraordinary variety of body types, life strategies, feeding mechanisms and striking adaptations. One of these adaptations is bioluminescence. Bioluminescence, the ability to produce light by living organisms, is a biological property that has evolved independently in many lineages across the tree of life (Harvey 1952; Haddock et al. 2010). Bioluminescent light results from a chemical reaction involving the oxidation of a light-emitting molecule— luciferin—by a specific enzyme—luciferase (Shimomura 2012). In some organisms, the luciferin is tightly bound to luciferase and oxygen forming a photoprotein, and light production is triggered when the photoprotein binds to a co-factor (Deheyn and Latz 2009). There are several types of photoproteins based on their chemical identity and the cofactor they require. For example, in coelenterates, ctenophores, and radiolarians, calcium is required to trigger luminescence, whereas the photoproteins of the bivalve Pholas and some polychaetes seem to bind to superoxide radicals, and the millipede Motyxia Advanced Access publication June 3, 2017 Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2017. This work is written by US Government employees and is in the public domain in the US. *Baruch College and The Graduate Center, PhD Program in Biology, City University of New York, 365 5th Ave, New York, NY 10010, USA; †Sackler Institute for Comparative Genomics, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192, USA; ‡Departamento de Biologıa (Zoologıa), Facultad de Ciencias, Universidad Aut onoma de Madrid, C/Darwin 2, Cantoblanco, Madrid, 28049, Spain 19 Bioluminescence in annelids example, in terrestrial environments bioluminescent light is generally yellow, whereas it has a green hue in shallow waters and it is usually blue in deep-sea habitats, corresponding to the wavelengths that propagate best in these environments (Haddock et al. 2010; Widder 2010). In a similar way, bioluminescent glows are thought to function as a lure or attraction signal, whether directed to prey or potential mates, whereas sudden flashes are generally associated with defensive functions, used to startle and confuse predators (Haddock et al. 2010). Within Annelids, bioluminescence has evolved independently in several lineages (Fig. 1) (Haddock et al. 2010; Shimomura 2012) possibly contributing to the high taxonomic diversity we observe today (Ellis and Oakley 2016) with almost 100 luminous species distributed in thirteen families (Fig. 1, Table 1). Their ecological diversity is also unparalleled, with species occupying a wide range of habitats including both terrestrial and marine ecosystems from coastal waters to the deep-sea, and both benthic and pelagic habitats from polar to tropical regions. Their taxonomic and ecological diversity is matched by the wide array of bioluminescent colors (Figs. 1 and 2, Table 1), including yellow light emitters which are extremely rare among marine taxa (Fig. 2E) (Widder 2010), and widely varying patterns, chemical reactions, and kinetics. We present the current state of knowledge regarding luminous annelids, particularly focusing on their taxonomic and ecological diversity and discussing the putative functions and chemistries of their bioluminescent systems. Diversity of luminous annelids: which worms glow? Approximately 98 luminous annelid species representing 45 genera have been reported so far, distributed in five clitellate families including Acanthodrilidae, Enchytraeidae, Lumbricidae, Megascolecidae, and Octochaetidae, and eight polychaete families, namely Acrocirridae, Chaetopteridae, Cirratulidae, Flabelligeridae, Polynoidae, Syllidae, Terebellidae, and Tomopteridae (Fig. 1, Table 1) (Harvey 1952; Herring 1978, 1987; Shimomura 2012). Among these, there are species that occupy an incredible variety of habitats and ecological niches and show a corresponding diversity of bioluminescent colors and patterns. In this section, we review the diversity of luminescent annelids both in terms of taxonomic and ecological diversity and provide information about their bioluminescent displays and patterns. requires ATP and magnesium to produce light (Shimomura 1985). It is estimated that bioluminescence has originated independently a (...truncated)