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

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 deep-sea, 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.

Molecular phylogeny ofOdontosyllis(Annelida, Syllidae): A recent and rapid radiation of marine bioluminescent worms

“…Pionosyllis (Haddock et al, 2010;Verdes and Gruber, 2017;Zörner and Fischer, 2007). The ancestral state reconstruction analyses we propose tracing the evolution of bioluminescence in Eusyllinae suggest that the capability to produce light evolved once within the group and was present in both the most recent common ancestor of extant Eusyllinae lineages, and the most recent common ancestor of Odontosyllis ( Figure 6).…”

“…Several Odontosyllis species show an impressive bioluminescent display during reproduction, that has captivated humans since Christopher Columbus approached the Bahamas in 1492 (Crawshay, 1935). Bioluminescence has evolved independently in several annelid lineages (Haddock et al, 2010;Verdes and Gruber, 2017), including remarkable species like the deep sea Swima bombiviridis that releases luminescent "bombs" (Osborn et al, 2009) or the pelagic tomopterids that emit yellow light, an extremely rare color among marine luminescent taxa (Widder, 2010). There are many other examples among the 98 luminous annelids reported so far, which occupy a variety of habitats from terrestrial to marine ecosystems, and display a wide range of bioluminescent colors associated with different functions, such as defense or intraspecific communication (Verdes and Gruber, 2017).…”

“…In the summer months, a few days after a full moon and shortly after sunset, the benthic marine worms leave the ocean floor and swim to the surface to reproduce. In most cases, females appear first and swim in circles while releasing gametes in a cloud of bright green luminous mucus that attracts the males, which dart towards the females to spawn (Galloway and Welch, 1911;Markert et al, 1961;Verdes and Gruber, 2017). This courtship ritual has been thoroughly described from a behavioral point of view (Fischer and Fischer, 1995;Gaston and Hall, 2000;Huntsman, 1948;Markert et al, 1961;Tsuji and Hill, 1983), but little is known about the basic chemistry of the bioluminescence system or the evolution of light production in Odontosyllis.…”

Building customizable auto-luminescent luciferase-based reporters in plants

“…Bioluminescence is one of nature's more spectacular tricks. It is used by a diverse set of organisms to achieve a broad range of goals such as attracting mates, scaring off predators and recruiting other creatures to spread spores 1,2,3,4,5 . The mechanism of light emission is broadly conserved: an enzymatic oxidation reaction by a luciferase enzyme turns a luciferin substrate into a high energy intermediate which decays to produce light 1 .…”

Plants with self-sustained luminescence

“…The caffeic acid cycle from fungi is one example of the many distinct luminescent systems found among evolutionary distant organisms, ranging from bacteria to protists to fungi and animals 17 . Biochemical characterization of these systems has demonstrated that light emission is achievable via multiple metabolic routes 18 . Several luciferases have been used as reporters of biomolecular processes, most notably firefly luciferase, various marine luciferases, such as Renilla, Gaussia, Oplophorus and others, and bacterial luciferase 19 .…”