Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 107; no. 5; pp. 2259 - 2264
• Main Authors: Wier, Andrew M, Nyholm, Spencer V, Mandel, Mark J, Massengo-Tiassé, R. Prisca, Schaefer, Amy L, Koroleva, Irina, Splinter-BonDurant, Sandra, Brown, Bartley, Manzella, Liliana, Snir, Einat, Almabrazi, Hakeem, Scheetz, Todd E, Bonaldo, Maria de Fatima, Casavant, Thomas L, Soares, M. Bento, Cronan, John E, Reed, Jennifer L, Ruby, Edward G, McFall-Ngai, Margaret J
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 02.02.2010; National Acad Sciences
• Subjects: Aliivibrio fischeri - genetics; Aliivibrio fischeri - metabolism; Aliivibrio fischeri - ultrastructure; Anaerobic respiration; Anaerobiosis; Animals; Bacteria; Biological Sciences; Chitin; Chitin - metabolism; Circadian Rhythm - genetics; Circadian Rhythm - physiology; Crustaceans; Decapodiformes - anatomy & histology; Decapodiformes - genetics; Decapodiformes - metabolism; Decapodiformes - microbiology; Diet; Epithelium; Fatty acids; Fermentation; Gene expression; Gene Expression Profiling; Gene expression regulation; Genes; Genes, Bacterial; glycerol; Gram-negative bacteria; Lipid Metabolism; Lipids; Metabolism; Microscopy, Electron, Transmission; Models, Biological; Molecular Sequence Data; Oligonucleotide Array Sequence Analysis; Proteins; Squid; Symbionts; Symbiosis; Symbiosis - genetics; Symbiosis - physiology; transcription (genetics); transcriptome; transmission electron microscopy; Vibrio fischeri
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.0909712107

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.