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Proc Natl Acad Sci U S A. 2019 Apr 16;116(16):7990-7999. doi: 10.1073/pnas.1819897116. Epub 2019 Mar 4.

Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression.

Author information

1
Pacific Biosciences Research Center, University of Hawai'i at Mānoa, Honolulu, HI 96822.
2
Department of Molecular Biosciences and Bioengineering, University of Hawai'i at Mānoa, Honolulu, HI 96822.
3
Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI 53706.
4
Department of Bacteriology, University of Wisconsin-Madison, Madison, WI 53706.
5
Pacific Biosciences Research Center, University of Hawai'i at Mānoa, Honolulu, HI 96822; mcfallng@hawaii.edu.

Abstract

The colonization of an animal's tissues by its microbial partners creates networks of communication across the host's body. We used the natural binary light-organ symbiosis between the squid Euprymna scolopes and its luminous bacterial partner, Vibrio fischeri, to define the impact of colonization on transcriptomic networks in the host. A night-active predator, E. scolopes coordinates the bioluminescence of its symbiont with visual cues from the environment to camouflage against moon and starlight. Like mammals, this symbiosis has a complex developmental program and a strong day/night rhythm. We determined how symbiont colonization impacted gene expression in the light organ itself, as well as in two anatomically remote organs: the eye and gill. While the overall transcriptional signature of light organ and gill were more alike, the impact of symbiosis was most pronounced and similar in light organ and eye, both in juvenile and adult animals. Furthermore, the presence of a symbiosis drove daily rhythms of transcription within all three organs. Finally, a single mutation in V. fischeri-specifically, deletion of the lux operon, which abrogates symbiont luminescence-reduced the symbiosis-dependent transcriptome of the light organ by two-thirds. In addition, while the gills responded similarly to light-organ colonization by either the wild-type or mutant, luminescence was required for all of the colonization-associated transcriptional responses in the juvenile eye. This study defines not only the impact of symbiont colonization on the coordination of animal transcriptomes, but also provides insight into how such changes might impact the behavior and ecology of the host.

KEYWORDS:

bioluminescence; daily rhythm; development; squid–vibrio; symbiosis

PMID:
30833394
DOI:
10.1073/pnas.1819897116

Conflict of interest statement

Conflict of interest statement: L.Z. and M.J.M.-N. are coauthors on a 2015 Comment article.

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