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Proc Natl Acad Sci U S A. 2019 Feb 19;116(8):3030-3035. doi: 10.1073/pnas.1817322116. Epub 2019 Jan 11.

Symbiotic organs shaped by distinct modes of genome evolution in cephalopods.

Author information

1
Pacific Biosciences Research Center, University of Hawaii, Honolulu, HI 96822.
2
Department of Microbiology and Cell Science, Space Life Science Lab, University of Florida, Merritt Island, FL 32953.
3
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269.
4
Department of Molecular Evolution and Development, University of Vienna, 1090 Vienna, Austria.
5
Ecology, Evolution, and Marine Biology Department, University of California, Santa Barbara, CA 93106.
6
Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Claude Bernard University Lyon 1, CNRS, UMR 5558, 69100 Villeurbanne, France.
7
Jackson Laboratory for Genomic Medicine, Farmington, CT 06032.
8
McDonnell Genome Institute, Washington University, St. Louis, MO 63108.
9
Molecular Genetics Unit, Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan.
10
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720.
11
Department of Energy, Joint Genome Institute, Walnut Creek, CA 94598.
12
Department of Molecular Evolution and Development, University of Vienna, 1090 Vienna, Austria; oleg.simakov@univie.ac.at jfoster@ufl.edu spencer.nyholm@uconn.edu.
13
Department of Microbiology and Cell Science, Space Life Science Lab, University of Florida, Merritt Island, FL 32953; oleg.simakov@univie.ac.at jfoster@ufl.edu spencer.nyholm@uconn.edu.
14
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269; oleg.simakov@univie.ac.at jfoster@ufl.edu spencer.nyholm@uconn.edu.

Abstract

Microbes have been critical drivers of evolutionary innovation in animals. To understand the processes that influence the origin of specialized symbiotic organs, we report the sequencing and analysis of the genome of Euprymna scolopes, a model cephalopod with richly characterized host-microbe interactions. We identified large-scale genomic reorganization shared between E. scolopes and Octopus bimaculoides and posit that this reorganization has contributed to the evolution of cephalopod complexity. To reveal genomic signatures of host-symbiont interactions, we focused on two specialized organs of E. scolopes: the light organ, which harbors a monoculture of Vibrio fischeri, and the accessory nidamental gland (ANG), a reproductive organ containing a bacterial consortium. Our findings suggest that the two symbiotic organs within E. scolopes originated by different evolutionary mechanisms. Transcripts expressed in these microbe-associated tissues displayed their own unique signatures in both coding sequences and the surrounding regulatory regions. Compared with other tissues, the light organ showed an abundance of genes associated with immunity and mediating light, whereas the ANG was enriched in orphan genes known only from E. scolopes Together, these analyses provide evidence for different patterns of genomic evolution of symbiotic organs within a single host.

KEYWORDS:

cephalopods; evolution; genomics; symbiosis; transcriptomics

Comment in

PMID:
30635418
PMCID:
PMC6386654
DOI:
10.1073/pnas.1817322116
[Indexed for MEDLINE]
Free PMC Article

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