Enlightenment of old ideas from new investigations: more questions regarding the evolution of bacteriogenic light organs in squids

Abstract

Bioluminescence is widespread among many different types of marine organisms. Metazoans contain two types of luminescence production, bacteriogenic (symbiotic with bacteria) or autogenic, via the production of a luminous secretion or the intrinsic properties of luminous cells. Several species in two families of squids, the Loliginidae and the Sepiolidae (Mollusca: Cephalopoda) harbor bacteriogenic light organs that are found central in the mantle cavity. These light organs are exceptional in function, that is, the morphology and the complexity suggests that the organ has evolved to enhance and direct light emission from bacteria that are harbored inside. Although light organs are widespread among taxa within the Sepiolidae, the origin and development of this important feature is not well studied. We compared light organ morphology from several closely related taxa within the Sepiolidae and combined molecular phylogenetic data using four loci (nuclear ribosomal 28S rRNA and the mitochondrial cytochrome c oxidase subunit I and 12S and 16S rRNA) to determine whether this character was an ancestral trait repeatedly lost among both families or whether it evolved independently as an adaptation to the pelagic and benthic lifestyles. By comparing other closely related extant taxa that do not contain symbiotic light organs, we hypothesized that the ancestral state of sepiolid light organs most likely evolved from part of a separate accessory gland open to the environment that allowed colonization of bacteria to occur and further specialize in the eventual development of the modern light organ.

Salinity and Temperature Effects on Physiological Responses of Vibrio fischeri from Diverse Ecological Niches

“…fischeri is a cosmopolitan microbe with a ubiquitous distribution in oceans, estuaries, brackish waters, and marine sediments throughout the world [37], as either part of free-living bacterioplankton or as a mutualistic symbiont [7,38]. Although most V. fischeri strains are "facultative" symbionts with cyclical free-living and mutualistic lifestyles, V. fischeri strains exist that persist strictly as members of the bacterioplankton and are symbiotically incompetent, essentially becoming obligately free-living [8].…”

“…For instance, Photobacterium leiognathi typically is more abundant as a free-living microbe in warmer waters; however, this species can be found as a symbiont in both temperate-water and tropical leiognathid fishes [7]. V. fischeri itself is usually a temperate-water species but can be found in hosts inhabiting both tropical and temperate waters [38]. This provides evidence that the distribution, ecology, and evolution of luminescent bacterial species in marine environments can be partially driven by symbiosis as opposed to abiotic factors.…”

Predation Response of Vibrio fischeri Biofilms to Bacterivorus Protists

“…Therefore, environmental fluctuations lead to considerable bacterial microdiversity and evolution, including evolution of a wide variety of pathogenic and facultative mutualistic strains. The latter include the bioluminescent bacterium V. fischeri, which exists in a free-living stage (seawater) or as a mutualist of sepiolid squids and monocentrid fishes (31)(32)(33).…”

Ultrastructure of Light Organs of Loliginid Squids with Insights into the Morphology of Bacteriogenic Light Organs

“…These complex organs, also known as photophores, have a variety of morphological characteristics, and range from groups of simple, light-producing cells, to specialized light organs with cells surrounded by reflectors, lenses, light guides, color filters, and muscles [2]. Bacteriogenic light organs have been well characterized in sepiolid squids, but a number of species in the family Loliginidae are also known to contain bacteriogenic light organs [3].Comparable in complexity to the compound eyes of many animals, light organs are able to readily adjust color, intensity, and angular distribution of light produced from within [4]. In oceanic cephalopods, photophores emit intrinsic luminescence (autogenic) with different spectra of light emanating from their own photocytes [5].…”

“…These complex organs, also known as photophores, have a variety of morphological characteristics, and range from groups of simple, light-producing cells, to specialized light organs with cells surrounded by reflectors, lenses, light guides, color filters, and muscles [2]. Bacteriogenic light organs have been well characterized in sepiolid squids, but a number of species in the family Loliginidae are also known to contain bacteriogenic light organs [3].…”