Journal article
Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis
Proceedings of the National Academy of Sciences - PNAS, Vol.107(5), pp.2259-2264
02/02/2010
DOI: 10.1073/pnas.0909712107
PMCID: PMC2836665
PMID: 20133870
Abstract
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.
Details
- Title: Subtitle
- Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis
- Creators
- Andrew M Wier - Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706, USASpencer V NyholmMark J MandelR Prisca Massengo-TiasséAmy L SchaeferIrina KorolevaSandra Splinter-BondurantBartley BrownLiliana ManzellaEinat SnirHakeem AlmabraziTodd E ScheetzMaria de Fatima BonaldoThomas L CasavantM Bento SoaresJohn E CronanJennifer L ReedEdward G RubyMargaret J McFall-Ngai
- Resource Type
- Journal article
- Publication Details
- Proceedings of the National Academy of Sciences - PNAS, Vol.107(5), pp.2259-2264
- Publisher
- United States
- DOI
- 10.1073/pnas.0909712107
- PMID
- 20133870
- PMCID
- PMC2836665
- ISSN
- 0027-8424
- eISSN
- 1091-6490
- Grant note
- R01 AI015650 / NIAID NIH HHS R01-AI15650 / NIAID NIH HHS R01 OD011024 / NIH HHS R37 AI050661 / NIAID NIH HHS R01-AI50661 / NIAID NIH HHS R01 AI050661 / NIAID NIH HHS R01 RR012294 / NCRR NIH HHS F32 GM078760 / NIGMS NIH HHS R01-RR12294 / NCRR NIH HHS
- Language
- English
- Date published
- 02/02/2010
- Academic Unit
- Roy J. Carver Department of Biomedical Engineering; Electrical and Computer Engineering; Ophthalmology and Visual Sciences
- Record Identifier
- 9983979976902771
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