Luminescent bacteria as Symbiont

Bioluminescence, which is the natural production of light by organisms, occurs in animals, fungi, protists and certain bacteria. Light is produced when the compound luciferin is oxidised. Larger organisms such as squid contain light organs where light production takes place, in smaller organisms such as bacteria, the whole organism luminesces. Over 90% of species which inhabit depths greater than 700m, are thought to possess the ability to bioluminescence. In most species, luminescence is produced by the animal, however in a minority, the light is produced by bacteria which function as symbionts of the animal within its light organs.

Bioluminescent symbiotic associations with luminous bacteria have been identified in  fish and and squids. The host animals utilise the luminescence for a variety of reasons. These include: predator avoidance (through counter-illumination and flashing), mating related signalling, attracting and locating prey and navigation in dark or low-light environments.

Luminous Bacteria

 Luminous bacteria are the most widely distributed light-emitting organisms with the majority existing in seawater and the rest living in the terrestrial or freshwater environment. While most species of luminescent bacteria are capable of living free, the majority are found in nature associated in symbiosis with host organisms (i.e., fishes, squids, crabs, nematodes, etc.). In symbiosis, the bacteria are nourished with readily available food sources for growth, and at the same time the host utilizes the adopted illumination to communicate, to attract prey, and to masquerade itself from predators.

 Figure 1. Pinecone fish utilize luminous bacteria, colonized in the ventral cavity, to illuminate the surroundings as well as for intra-species communication.

 Figure 2. The deep sea Angler fish carries luminous bacteria in a light emitting rod, which attracts prey to the front of its mouth.

            There are certain species of luminescent bacteria, which are obligatory symbionts, requiring unique nutritional supplements, which are exclusively available from the host. Though their presence have been detected, they are not separable from their host, and therefore are unable to be cultured in the laboratory for further study.

            There are three major genera, into which most luminous bacteria are classified; Photobacterium, Vibrio, and Photorhabdus. Species existing in the marine environment are mainly categorized into the Photobacterium and Vibrio genera, and the terrestrial species are classified into the Photorhabdus (previously designated as Xenorhabdus) genus. Species within the Photobacterium genus are generally light organ symbionts of marine animals, whereas the Vibrio species exist as free-living forms as well as symbionts in the sea.

 

 Figure 3. Luminous bacteria reside in symbiosis on a pair of light organs in the mantle body of the squid. Utilization of the illumination function is believed to frighten nearby predators, allowing the squid to escape.

 

Many luminous bacteria are parasitic, with Photobacterium and Vibrio families infecting marine crustacea, and Photorhabdus luminescens infecting terrestrial insects, such as caterpillars, with nematodes as the intermediate host for the bacteria.  

        For luminous bacteria residing within the gut tracts of marine animals, the extra-cellular chitinase produced on the cell wall of all luminous bacteria facilitate the decomposition of the ingested chitin (e.g., from the exoskeletons of crustacea).

 

Figure 5. Luminous bacteria are non-specific parasites of crustacea. The exoskeletons of Tanner crabs are the sites of colonization of luminous bacteria, whose infection causes lesions on the surface of its appendages.

      Majority of luminous bacteria are  marine forms, requiring salt for growth and luminescence, and are widely distributed throughout the oceans of the world. The most common are Vibrio and Photobacterium species. While luminous bacteria come in various shapes, they do not form clusters or chains, as do many other bacteria. The light of an individual bacterium cannot be seen with the naked eye, but the light from a liquid or agar culture containing billions of bacteria is readily visible. The light is bluish and continuous. Many luminous bacteria live in the light organs of fish and squids, without adversely affecting their hosts.

            All luminous bacteria are rod-shaped, gram-negative microorganisms with flagella. Each species of luminous bacteria differs in a number of properties, including the growing  conditions (nutritional requirements and growth temperature), and the reaction kinetics of the luciferase involved in light generation. Luminous bacteria are also facultative anaerobes capable of growth when the supply of molecular oxygen is limited. Despite the physiological diversity among different species of luminous bacteria, all luminescent microorganisms utilize highly homologous biochemical machineries including bacterial luciferase and other enzymes that supply and regenerate the substrates of bacterial luciferase, to produce light. This light-producing molecular machinery are tightly regulated under a central signalling pathway.     

Hosts

1. Squid.

Bioluminescent squid species contain at least three species of luminous bacteria Vibrio fischeri  V. logei and Photobacterium leiognathi located in specialised strucrutres called the light organs. The light organs  are bilobed organs found within the mantle cavity, adjacent to the ink sac. Squids acquire their symbiotic luminous bacteria by horizontal transfer from the surrounding seawater.

2.  Fish.

Bioluminescent fish species contain at least three identified species of luminous bacteria in symbiotic associations; Vibrio fischeri, Photobacterium leiognathi and Photobacterium phosphoreum. The symbiotic bacteria are extra cellular and inhabit tubules and canals of the fish’s light organ. The fish keep a high density of bacteria present in their light organ, which leads to continuous illumination of the organ. The light organ in fish may be located in various places. Light organs have a rich blood supply that nourishes and maintains the luminous bacteria. Each fish species becomes infected with a specific bacterial type. 

Development of the light organ in some fish (Monocentris japonicus) may require first the acquiring of symbionts (V. fischeri). As with squid, fish also acquire their luminescent symbionts through horizontal transfer from the surrounding seawater. It has been found in studies that the fish’s offspring are without symbiotic bacteria (aposymbiotic) at hatching and require the presence of adult fish to gain symbionts, due to the exudation of bacteria into the surrounding seawater from the adults. The offsprings kept apart from adult fish fail to acquire luminescence.

Depending upon the the particular species, the organs containing the luminescent bacteria may be localized near the eye, abdomen, rectum or jaw. The bacteria-filled organ is continuously luminous, but the light can be controlled either by contraction and expansion of melanophores, or pigment granules or mechanically by a black membrane that may be drawn over the organ. In such cases, fish can manipulate the light organ containing the bacteria so as to emit flashes of light. The flashlight fish Photoblepharon can shut off its light by drawing a dark curtain, like an eyelid over its light organ. Anomalops has the light organ which can be rotated like an eyeball, almost 180⁰. The light is reflected inward and is hidden. 

Photoblepharon and Anomalops are nocturnal, use the light organs as flash light or head lamp, for the schooling behaviour, since they are gregarious in nature and also to repel predators.  

Mutualistic associations of luminescent bacteria with deep sea fishes, permits species recognition, in mate recognition (since they occur in only one sex), as search lights, and also to lure prey and communicate with other fish.

Significance of Bioluminescence Symbioses.

Bioluminescence symbioses are highly significant examples of symbioses in the marine environment. One significant aspect of bioluminescent symbioses is the small minority of species it occurs in.

In most bacteria-animal symbiotic associations, the host animal benefits from the association by the acquiring of nutrients (e.g. through nitrogen fixation by the bacteria) which are used for growth purposes. However, in bioluminescence symbioses, the host benefits through the acquisition of light, which is used for a variety of purposes, not directly linked with growth. In squid, these may be to camouflage or to scare other organisms through fright. In fish, these may be to attract prey, become invisible and to communicate. The fish/squid in turn provide the bacteria with nutrients, oxygen and shelter within the light organ.

Another significant ecological aspect of bioluminescent symbiotic associations is the extent of influence the host animal has on the bacterial symbionts. The host animals exert an influence on the bacteria in a number of ways. There is a very significant effect of host control on the bacteria as the host regulates the supply of oxygen and/or nutrients to the bacteria. The influence bacteria exert on their hosts is of less significance. The fish/squid survive just as well without its luminous symbionts as animals with theirs. This is in contrast to most other bacterial symbiotic associations in the marine environment, where the bacteria would have a much greater influence on the host as the host would be nutritionally dependant on the bacteria.

The bioluminescent symbiotic associations, and their mechanisms, are very unique. The greatest significance of these mechanisms is their ecological uniqueness in the world of bacterial symbiotic associations.