Bacterial bioluminescence as a lure for marine zooplankton and fish

Abstract

The benefits of bioluminescence for nonsymbiotic marine bacteria have not been elucidated fully. One of the most commonly cited explanations, proposed more than 30 y ago, is that bioluminescence augments the propagation and dispersal of bacteria by attracting fish to consume the luminous material. This hypothesis, based mostly on the prevalence of luminous bacteria in fish guts, has not been tested experimentally. Here we show that zooplankton that contacts and feeds on the luminescent bacterium Photobacterium leiognathi starts to glow, and demonstrate by video recordings that glowing individuals are highly vulnerable to predation by nocturnal fish. Glowing bacteria thereby are transferred to the nutritious guts of fish and zooplankton, where they survive digestion and gain effective means for growth and dispersal. Using bioluminescence as bait appears to be highly beneficial for marine bacteria, especially in food-deprived environments of the deep sea.B ioluminescence is common in the marine environment, occurring in numerous organisms, from bacteria to invertebrates and fish (1, 2). Bacterial bioluminescence occurs as a continuous glow in the presence of oxygen at cell concentrations exceeding quorum-sensing levels (3-6). Luminous bacteria occur free-living in seawater (7,8), in symbiotic associations with marine organisms (most notably fish and squids; see refs. 7 and 8 and references therein), as saprophytes on suspended organic material such as marine snow (9, 10), as a major component of fecal pellets (11-13), and as parasites on crustaceans (14).Although the adaptive benefits of energetically costly bioluminescence in symbiotic bacteria are well understood (e.g., 7, 15), those benefits in nonsymbiotic bacteria and those living as ectoparasites on zooplankton are less obvious. Several different physiological and biochemical functions of bacterial bioluminescence have been proposed (7,(16)(17)(18)(19)(20), focusing mostly on antioxidative activity, enhanced DNA repair, and UV resistance, although the validity of some of these hypotheses has been questioned (21).An ecological function in propagation and dispersal also has been postulated (6,7,22). According to this hypothesis (hereafter, "bait hypothesis"), the bacteria, by glowing, visually mark the presence of a food particle for fish in order to get into their nutritious guts. So far, this hypothesis was supported by circumstantial evidence showing that luminous bacteria thrive in and survive passage through fish guts (7,12,23,24). Here we propose that the mechanism underlying the bait hypothesis is based on the following steps: (i) Quorum sensing assures that bacterial bioluminescence is a reliable signal of the presence of food aggregates, e.g., marine snow; (ii) zooplankton is attracted to luminous particles and grazes on the bacteria-rich organic matter; (iii) because of its contact with or ingestion of the luminous bacteria, the zooplankton itself becomes glowing; (iv) the glowing zooplankton is detected readily and consumed by fish; (v) once in the ...

A Small Number of Phylogenetically Distinct Clonal Complexes Dominate a Coastal Vibrio cholerae Population

“…Previous studies in Chesapeake Bay, a brackish water habitat similar to Oyster Pond, have found the presence of bioluminescence in around 50% of all isolated strains and, based on clustering by phenotypic traits, hypothesized the presence of the lux operon to be an ecologically relevant trait of environmental nontoxigenic branches in the phylogeny of V. cholerae (19,52). The bioluminescence trait has been linked to the colonization of zooplankton, which in an illuminated state makes easy prey for visually oriented predators, thus enabling bioluminescent bacteria to invade the nutrient-rich gut regions of vertebrate predators (19,53). CC1 strains also harbor the ability to take up choline and convert it to betaine (through the action of the betTIBA operon, shared with sister taxa CC2, RC385, and VL426).…”

Vibrio fischeri Metabolism

“…This research tested the long-held hypothesis that light production acts as a lure for fish and allows the bacterium to gain access to the nutrient-rich fish intestine (Zarubin, Belkin, Ionescu, & Genin, 2012). For example, a recent study explored the role of bioluminescence in the bacterium Photobacterium leiognathi.…”

Towards more efficient longline fisheries: fish feeding behaviour, bait characteristics and development of alternative baits

“…A recent laboratory study showed that the nocturnal ringtail cardinalfish (Apogon annularis) was more attracted to zooplankton which had fed on luminescent bacteria and subsequently started to glow (Zarubin et al 2012). A field study found catch rates that were 1.2 times as high in tuna, and up to 4.8 times as high in several bottom-dwelling species when a bait dipped in a luminescent solution was used (Makiguchi et al 1980).…”