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The round goby genome provides insights into mechanisms that may facilitate biological invasions

BACKGROUND: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection...

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Autores principales: Adrian-Kalchhauser, Irene, Blomberg, Anders, Larsson, Tomas, Musilova, Zuzana, Peart, Claire R., Pippel, Martin, Solbakken, Monica Hongroe, Suurväli, Jaanus, Walser, Jean-Claude, Wilson, Joanna Yvonne, Alm Rosenblad, Magnus, Burguera, Demian, Gutnik, Silvia, Michiels, Nico, Töpel, Mats, Pankov, Kirill, Schloissnig, Siegfried, Winkler, Sylke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988351/
https://www.ncbi.nlm.nih.gov/pubmed/31992286
http://dx.doi.org/10.1186/s12915-019-0731-8
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author Adrian-Kalchhauser, Irene
Blomberg, Anders
Larsson, Tomas
Musilova, Zuzana
Peart, Claire R.
Pippel, Martin
Solbakken, Monica Hongroe
Suurväli, Jaanus
Walser, Jean-Claude
Wilson, Joanna Yvonne
Alm Rosenblad, Magnus
Burguera, Demian
Gutnik, Silvia
Michiels, Nico
Töpel, Mats
Pankov, Kirill
Schloissnig, Siegfried
Winkler, Sylke
author_facet Adrian-Kalchhauser, Irene
Blomberg, Anders
Larsson, Tomas
Musilova, Zuzana
Peart, Claire R.
Pippel, Martin
Solbakken, Monica Hongroe
Suurväli, Jaanus
Walser, Jean-Claude
Wilson, Joanna Yvonne
Alm Rosenblad, Magnus
Burguera, Demian
Gutnik, Silvia
Michiels, Nico
Töpel, Mats
Pankov, Kirill
Schloissnig, Siegfried
Winkler, Sylke
author_sort Adrian-Kalchhauser, Irene
collection PubMed
description BACKGROUND: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales and present promising case studies to understand factors involved the impressive ability of some species to colonize novel environments. We seize the unique opportunity presented by the round goby invasion to study genomic substrates potentially involved in colonization success. RESULTS: We report a highly contiguous long-read-based genome and analyze gene families that we hypothesize to relate to the ability of these fish to deal with novel environments. The analyses provide novel insights from the large evolutionary scale to the small species-specific scale. We describe expansions in specific cytochrome P450 enzymes, a remarkably diverse innate immune system, an ancient duplication in red light vision accompanied by red skin fluorescence, evolutionary patterns of epigenetic regulators, and the presence of osmoregulatory genes that may have contributed to the round goby’s capacity to invade cold and salty waters. A recurring theme across all analyzed gene families is gene expansions. CONCLUSIONS: The expanded innate immune system of round goby may potentially contribute to its ability to colonize novel areas. Since other gene families also feature copy number expansions in the round goby, and since other Gobiidae also feature fascinating environmental adaptations and are excellent colonizers, further long-read genome approaches across the goby family may reveal whether gene copy number expansions are more generally related to the ability to conquer new habitats in Gobiidae or in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0731-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-69883512020-02-03 The round goby genome provides insights into mechanisms that may facilitate biological invasions Adrian-Kalchhauser, Irene Blomberg, Anders Larsson, Tomas Musilova, Zuzana Peart, Claire R. Pippel, Martin Solbakken, Monica Hongroe Suurväli, Jaanus Walser, Jean-Claude Wilson, Joanna Yvonne Alm Rosenblad, Magnus Burguera, Demian Gutnik, Silvia Michiels, Nico Töpel, Mats Pankov, Kirill Schloissnig, Siegfried Winkler, Sylke BMC Biol Research Article BACKGROUND: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales and present promising case studies to understand factors involved the impressive ability of some species to colonize novel environments. We seize the unique opportunity presented by the round goby invasion to study genomic substrates potentially involved in colonization success. RESULTS: We report a highly contiguous long-read-based genome and analyze gene families that we hypothesize to relate to the ability of these fish to deal with novel environments. The analyses provide novel insights from the large evolutionary scale to the small species-specific scale. We describe expansions in specific cytochrome P450 enzymes, a remarkably diverse innate immune system, an ancient duplication in red light vision accompanied by red skin fluorescence, evolutionary patterns of epigenetic regulators, and the presence of osmoregulatory genes that may have contributed to the round goby’s capacity to invade cold and salty waters. A recurring theme across all analyzed gene families is gene expansions. CONCLUSIONS: The expanded innate immune system of round goby may potentially contribute to its ability to colonize novel areas. Since other gene families also feature copy number expansions in the round goby, and since other Gobiidae also feature fascinating environmental adaptations and are excellent colonizers, further long-read genome approaches across the goby family may reveal whether gene copy number expansions are more generally related to the ability to conquer new habitats in Gobiidae or in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-019-0731-8) contains supplementary material, which is available to authorized users. BioMed Central 2020-01-28 /pmc/articles/PMC6988351/ /pubmed/31992286 http://dx.doi.org/10.1186/s12915-019-0731-8 Text en © The Author(s). 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Adrian-Kalchhauser, Irene
Blomberg, Anders
Larsson, Tomas
Musilova, Zuzana
Peart, Claire R.
Pippel, Martin
Solbakken, Monica Hongroe
Suurväli, Jaanus
Walser, Jean-Claude
Wilson, Joanna Yvonne
Alm Rosenblad, Magnus
Burguera, Demian
Gutnik, Silvia
Michiels, Nico
Töpel, Mats
Pankov, Kirill
Schloissnig, Siegfried
Winkler, Sylke
The round goby genome provides insights into mechanisms that may facilitate biological invasions
title The round goby genome provides insights into mechanisms that may facilitate biological invasions
title_full The round goby genome provides insights into mechanisms that may facilitate biological invasions
title_fullStr The round goby genome provides insights into mechanisms that may facilitate biological invasions
title_full_unstemmed The round goby genome provides insights into mechanisms that may facilitate biological invasions
title_short The round goby genome provides insights into mechanisms that may facilitate biological invasions
title_sort round goby genome provides insights into mechanisms that may facilitate biological invasions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6988351/
https://www.ncbi.nlm.nih.gov/pubmed/31992286
http://dx.doi.org/10.1186/s12915-019-0731-8
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