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      Symbiotic organs shaped by distinct modes of genome evolution in cephalopods

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          Animal–microbe associations are critical drivers of evolutionary innovation, yet the origin of specialized symbiotic organs remains largely unexplored. We analyzed the genome of Euprymna scolopes, a model cephalopod, and observed large-scale genomic reorganizations compared with the ancestral bilaterian genome. We report distinct evolutionary signatures within the two symbiotic organs of E. scolopes, the light organ (LO) and the accessory nidamental gland (ANG). The LO evolved through subfunctionalization of genes expressed in the eye, indicating a deep evolutionary link between these organs. Alternatively, the ANG was enriched in novel, species-specific orphan genes suggesting these two tissues originated via different evolutionary strategies. These analyses represent the first genomic insights into the evolution of multiple symbiotic organs within a single animal host.

          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.

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          Most cited references29

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          Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis

          The root nodule symbiosis of plants with nitrogen-fixing bacteria impacts global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of ten plant species covering the diversity of nodule morphotypes, bacterial symbionts and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION (NIN) in ten out of 13 genomes of non-nodulating species within this clade. The discovery that multiple independent losses shaped the present day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so far underestimated selection pressure against this symbiosis.
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            Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules: Extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators.

            Cephalopods are extraordinary molluscs equipped with vertebrate-like intelligence and a unique buoyancy system for locomotion. A growing body of evidence from the fossil record, embryology and Bayesian molecular divergence estimations provides a comprehensive picture of their origins and evolution. Cephalopods evolved during the Cambrian (∼530 Ma) from a monoplacophoran-like mollusc in which the conical, external shell was modified into a chambered buoyancy apparatus. During the mid-Palaeozoic (∼416 Ma) cephalopods diverged into nautiloids and the presently dominant coleoids. Coleoids (i.e. squids, cuttlefish and octopods) internalised their shells and, in the late Palaeozoic (∼276 Ma), diverged into Vampyropoda and the Decabrachia. This shell internalisation appears to be a unique evolutionary event. In contrast, the loss of a mineralised shell has occurred several times in distinct coleoid lineages. The general tendency of shell reduction reflects a trend towards active modes of life and much more complex behaviour. Copyright © 2011 WILEY Periodicals, Inc.
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              Reflectins: the unusual proteins of squid reflective tissues.

              A family of unusual proteins is deposited in flat, structural platelets in reflective tissues of the squid Euprymna scolopes. These proteins, which we have named reflectins, are encoded by at least six genes in three subfamilies and have no reported homologs outside of squids. Reflectins possess five repeating domains, which are highly conserved among members of the family. The proteins have a very unusual composition, with four relatively rare residues (tyrosine, methionine, arginine, and tryptophan) comprising approximately 57% of a reflectin, and several common residues (alanine, isoleucine, leucine, and lysine) occurring in none of the family members. These protein-based reflectors in squids provide a marked example of nanofabrication in animal systems.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                19 February 2019
                11 January 2019
                11 January 2019
                : 116
                : 8
                : 3030-3035
                Affiliations
                [1] aPacific Biosciences Research Center, University of Hawaii , Honolulu, HI 96822;
                [2] bDepartment of Microbiology and Cell Science, Space Life Science Lab, University of Florida , Merritt Island, FL 32953;
                [3] cDepartment of Molecular and Cell Biology, University of Connecticut , Storrs, CT 06269;
                [4] dDepartment of Molecular Evolution and Development, University of Vienna , 1090 Vienna, Austria;
                [5] eEcology, Evolution, and Marine Biology Department, University of California, Santa Barbara , CA 93106;
                [6] fLaboratoire de Biométrie et Biologie Evolutive, Université de Lyon , Claude Bernard University Lyon 1, CNRS, UMR 5558, 69100 Villeurbanne, France;
                [7] gJackson Laboratory for Genomic Medicine , Farmington, CT 06032;
                [8] hMcDonnell Genome Institute, Washington University , St. Louis, MO 63108;
                [9] iMolecular Genetics Unit, Okinawa Institute of Science and Technology , Okinawa 904-0495, Japan;
                [10] jDepartment of Molecular and Cell Biology, University of California, Berkeley , CA 94720;
                [11] kDepartment of Energy, Joint Genome Institute , Walnut Creek, CA 94598
                Author notes
                1To whom correspondence may be addressed. Email: oleg.simakov@ 123456univie.ac.at , jfoster@ 123456ufl.edu , or spencer.nyholm@ 123456uconn.edu .

                Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved December 11, 2018 (received for review October 9, 2018)

                Author contributions: M.B., M.M.-N., O.S., J.S.F., and S.V.N. designed research; M.B., G.C., S.J.M., A.M.S., S.M.-G., M.S.P., T.H.O., N.K., E.J.K., A.J.C., H.N., S.L., I.G.-F., P.M., E.S., G.W., D.S.R., O.S., J.S.F., and S.V.N. performed research; S.M.-G., M.S.P., T.H.O., N.K., E.J.K., A.J.C., H.N., S.L., P.M., E.S., G.W., D.S.R., M.M.-N., O.S., J.S.F., and S.V.N. contributed new reagents/analytic tools; M.B., G.C., S.J.M., H.S., A.M.S., H.N., S.L., P.M., E.S., G.W., D.S.R., O.S., J.S.F., and S.V.N. analyzed data; and M.B., G.C., S.J.M., H.S., A.M.S., S.M.-G., M.S.P., T.H.O., N.K., E.J.K., A.J.C., H.N., S.L., I.G.-F., P.M., E.S., G.W., D.S.R., M.M.-N., O.S., J.S.F., and S.V.N. wrote the paper.

                Author information
                http://orcid.org/0000-0002-4478-915X
                Article
                201817322
                10.1073/pnas.1817322116
                6386654
                30635418
                fd193271-bb62-4080-844a-b3abe9c80283
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 6
                Funding
                Funded by: HHS | National Institutes of Health (NIH) 100000002
                Award ID: R01-AI50661
                Award Recipient : Margaret J. McFall-Ngai
                Funded by: HHS | National Institutes of Health (NIH) 100000002
                Award ID: R01-OD11024
                Award Recipient : Margaret J. McFall-Ngai
                Funded by: University of Wisconsin-Madison (UW) 100007015
                Award ID: none
                Award Recipient : Margaret J. McFall-Ngai
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: IOS 1557914
                Award Recipient : Spencer V. Nyholm
                Funded by: National Aeronautics and Space Administration (NASA) 100000104
                Award ID: NNX13AM44G
                Award Recipient : Jamie S. Foster
                Funded by: University of Connecticut (UCONN) 100007710
                Award ID: none
                Award Recipient : Spencer V. Nyholm
                Funded by: Okinawa Institute of Science and Technology
                Award ID: none
                Award Recipient : Daniel S. Rokhsar
                Funded by: Austrian Science Fund (FWF) 501100002428
                Award ID: P30686-B29
                Award Recipient : Oleg Simakov
                Categories
                Biological Sciences
                Evolution
                From the Cover

                cephalopods,symbiosis,evolution,genomics,transcriptomics
                cephalopods, symbiosis, evolution, genomics, transcriptomics

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