Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis.
Mechanisms for controlling symbiont populations are critical for maintaining the associations that exist between a host and its microbial partners. We describe here the transcriptional, metabolic, and ultrastructural characteristics of a diel rhythm that occurs in the symbiosis between the squid Euprymna scolopes and the luminous bacterium Vibrio fischeri. The rhythm is driven by the host's expulsion from its light-emitting organ of most of the symbiont population each day at dawn. The transcriptomes of both the host epithelium that supports the symbionts and the symbiont population itself were characterized and compared at four times over this daily cycle. The greatest fluctuation in gene expression of both partners occurred as the day began. Most notable was an up-regulation in the host of >50 cytoskeleton-related genes just before dawn and their subsequent down-regulation within 6 h. Examination of the epithelium by TEM revealed a corresponding restructuring, characterized by effacement and blebbing of its apical surface. After the dawn expulsion, the epithelium reestablished its polarity, and the residual symbionts began growing, repopulating the light organ. Analysis of the symbiont transcriptome suggested that the bacteria respond to the effacement by up-regulating genes associated with anaerobic respiration of glycerol; supporting this finding, lipid analysis of the symbionts' membranes indicated a direct incorporation of host-derived fatty acids. After 12 h, the metabolic signature of the symbiont population shifted to one characteristic of chitin fermentation, which continued until the following dawn. Thus, the persistent maintenance of the squid-vibrio symbiosis is tied to a dynamic diel rhythm that involves both partners.
Wier
Andrew M
AM
Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706, USA.
Nyholm
Spencer V
SV
Mandel
Mark J
MJ
Massengo-Tiassé
R Prisca
RP
Schaefer
Amy L
AL
Koroleva
Irina
I
Splinter-Bondurant
Sandra
S
Brown
Bartley
B
Manzella
Liliana
L
Snir
Einat
E
Almabrazi
Hakeem
H
Scheetz
Todd E
TE
Bonaldo
Maria de Fatima
Mde F
Casavant
Thomas L
TL
Soares
M Bento
MB
Cronan
John E
JE
Reed
Jennifer L
JL
Ruby
Edward G
EG
McFall-Ngai
Margaret J
MJ
D048908:Aliivibrio fischeri / Q000235:genetics* / Q000378:metabolism* / Q000648:ultrastructure; D000693:Anaerobiosis; D000818:Animals; D002686:Chitin / Q000378:metabolism; D002940:Circadian Rhythm / Q000235:genetics / Q000502:physiology; D049832:Decapodiformes / Q000033:anatomy & histology / Q000235:genetics* / Q000378:metabolism / Q000382:microbiology*; D004032:Diet; D020869:Gene Expression Profiling; D005798:Genes, Bacterial; D050356:Lipid Metabolism; D046529:Microscopy, Electron, Transmission; D008954:Models, Biological; D008969:Molecular Sequence Data; D020411:Oligonucleotide Array Sequence Analysis; D013559:Symbiosis / Q000235:genetics* / Q000502:physiology*
D002686:Chitin