A new study published online in the journal mBio is the first to show that a bioluminescent bacterium known as Vibrio fischeri regulates a daily rhythm of the Hawaiian bobtail squid (Euprymna scolopes).
The Hawaiian bobtail squid seems to have its biological rhythms regulated by a symbiotic bacterium (William Ormerod / Margaret McFall-Ngai)
The study reveals that the light generated by the colonizing bacterium triggers a genetic cascade in the cells of the squid light organ, which, in turn, control the daily cycle of biological activity typically synchronized by environmental cues such as sunlight.
“Instead of environmental light, this animal responds and cycles in response to the luminescence from its own light organ,” said senior author Prof McFall-Ngai from the University of Wisconsin-Madison.
Circadian rhythm in humans and other animals is governed by an internal or ‘biological clock’ with a cycle of about 24 hours and seems to be regulated largely by exposure to light and darkness. It is responsible for sleep cycles and other physiological and metabolic functions. Its most visible manifestations in humans occur in things like jet lag and the effects of night work shifts. Disrupting the daily cycle can have serious health consequences, including sleep and immune system disorders, and conditions like seasonal affective disorder.
At the molecular level, circadian rhythm is driven by a set of ‘clock genes’ and their relatives.
“This animal has a light-producing system in an organ in the middle of the body,” Prof McFall-Ngai said. “The bacteria in the light organ are luminous, and their luminescence affects the expression of a clock gene known as ‘cry’ in the cells of the light organ that are interacting with these luminous bacteria.”
The squid spends its nights foraging near the ocean surface. It uses the light organ as a sort of cloaking device to fool predators lurking below. At daybreak, it expels or vents 90 percent of the glowing bacteria and burrows into the sand where it can safely sleep until nightfall when, with a new crop of bacteria, it resumes its nocturnal foraging.
In the squid, the daily cycling of the cry genes found in the cells of the light organ are triggered by the light from the colonizing luminescent bacteria, making it a neat model to understand the interplay of a symbiont bacterium and the biological functions of its host.
Top left: juvenile E. scolopes, e – eyes, lo – light organ, seen through ventral mantle tissue. Top right: a light micrograph of a cross section of the juvenile light organ. The interior of the organ contains three epithelium-lined crypts, 1–3, each harboring bacteria in the crypt lumen. Surrounding the light organ and controlling light emission from the organ into the environment are the ink sac – is, and reflector – r, hg – hindgut. Bottom: light cycles experienced by E. scolopes. The squid is exposed to bright exogenous light – Daylight, during its diurnal quiescent period and bacterial luminescence of the light organ – Bioluminescence, during the night, when the host is active (Heath-Heckman EAC et al)
“In humans, the genes expressed in the gut are on a profound circadian rhythm run by the clock genes,” Prof McFall-Ngai explained. “Everything in the human gut is on a rhythm. Perhaps the thousands of bacteria there also govern the rhythms of the gut, just as the luminous bacteria partner of the squid sets the rhythms in the light organ.
“In the squid, we have one host and one microbe, and we can manipulate the microbe genetically and the whole system experimentally, which provides much more resolution than can be done in studies of the human gut.”
Prof McFall-Ngai’s team assessed the expression of the cry gene with and without bacteria present, and also with mutant bacteria incapable of producing light. Their results showed for the squid’s clock genes to be expressed in a rhythm, light from the bacterium is required.
While the study adds insight into the importance of biological rhythms for an animal’s well being, the most astonishing insight is that an animal’s circadian rhythm and the molecular switches that control it can be governed by a symbiotic microbe.
“We’re beginning to realize that circadian rhythms are really important for health and that microbes are important for everything,” Prof McFall-Ngai concluded.
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Bibliographic information: Heath-Heckman EAC et al. 2013. Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-vibrio symbiosis. mBio 4 (2):e00167-13; doi: 10.1128/mBio.00167-13
