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

Abstract 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 s...

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Main Authors: Irene Adrian-Kalchhauser, Anders Blomberg, Tomas Larsson, Zuzana Musilova, Claire R. Peart, Martin Pippel, Monica Hongroe Solbakken, Jaanus Suurväli, Jean-Claude Walser, Joanna Yvonne Wilson, Magnus Alm Rosenblad, Demian Burguera, Silvia Gutnik, Nico Michiels, Mats Töpel, Kirill Pankov, Siegfried Schloissnig, Sylke Winkler
Format: Article
Language:English
Published: BMC 2020-01-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-019-0731-8
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spelling doaj-aa587e2fe0c94578a07507f574fb279e2021-01-31T16:18:45ZengBMCBMC Biology1741-70072020-01-0118113310.1186/s12915-019-0731-8The round goby genome provides insights into mechanisms that may facilitate biological invasionsIrene Adrian-Kalchhauser0Anders Blomberg1Tomas Larsson2Zuzana Musilova3Claire R. Peart4Martin Pippel5Monica Hongroe Solbakken6Jaanus Suurväli7Jean-Claude Walser8Joanna Yvonne Wilson9Magnus Alm Rosenblad10Demian Burguera11Silvia Gutnik12Nico Michiels13Mats Töpel14Kirill Pankov15Siegfried Schloissnig16Sylke Winkler17Program Man-Society-Environment, Department of Environmental Sciences, University of BaselDepartment of Chemistry and Molecular Biology, University of GothenburgDepartment of Marine Sciences, University of GothenburgDepartment of Zoology, Charles UniversityDivision of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität MünchenMax Planck Institute of Molecular Cell Biology and GeneticsCentre for Ecological and Evolutionary Synthesis, University of OsloInstitute for Genetics, University of CologneGenetic Diversity Centre, ETHDepartment of Biology, McMaster UniversityDepartment of Chemistry and Molecular Biology, University of GothenburgDepartment of Zoology, Charles UniversityBiocenter, University of BaselInstitute of Evolution and Ecology, University of TuebingenUniversity of Bern, Institute for Fish and Wildlife HealthDepartment of Biology, McMaster UniversityResearch Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Max Planck Institute of Molecular Cell Biology and GeneticsAbstract 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.https://doi.org/10.1186/s12915-019-0731-8PacBioNeogobius melanostomusInvasive speciesFishGenomicsEvolution
collection DOAJ
language English
format Article
sources DOAJ
author Irene Adrian-Kalchhauser
Anders Blomberg
Tomas Larsson
Zuzana Musilova
Claire R. Peart
Martin Pippel
Monica Hongroe Solbakken
Jaanus Suurväli
Jean-Claude Walser
Joanna Yvonne Wilson
Magnus Alm Rosenblad
Demian Burguera
Silvia Gutnik
Nico Michiels
Mats Töpel
Kirill Pankov
Siegfried Schloissnig
Sylke Winkler
spellingShingle Irene Adrian-Kalchhauser
Anders Blomberg
Tomas Larsson
Zuzana Musilova
Claire R. Peart
Martin Pippel
Monica Hongroe Solbakken
Jaanus Suurväli
Jean-Claude Walser
Joanna Yvonne Wilson
Magnus Alm Rosenblad
Demian Burguera
Silvia Gutnik
Nico Michiels
Mats Töpel
Kirill Pankov
Siegfried Schloissnig
Sylke Winkler
The round goby genome provides insights into mechanisms that may facilitate biological invasions
BMC Biology
PacBio
Neogobius melanostomus
Invasive species
Fish
Genomics
Evolution
author_facet Irene Adrian-Kalchhauser
Anders Blomberg
Tomas Larsson
Zuzana Musilova
Claire R. Peart
Martin Pippel
Monica Hongroe Solbakken
Jaanus Suurväli
Jean-Claude Walser
Joanna Yvonne Wilson
Magnus Alm Rosenblad
Demian Burguera
Silvia Gutnik
Nico Michiels
Mats Töpel
Kirill Pankov
Siegfried Schloissnig
Sylke Winkler
author_sort Irene Adrian-Kalchhauser
title 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_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_sort round goby genome provides insights into mechanisms that may facilitate biological invasions
publisher BMC
series BMC Biology
issn 1741-7007
publishDate 2020-01-01
description Abstract 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.
topic PacBio
Neogobius melanostomus
Invasive species
Fish
Genomics
Evolution
url https://doi.org/10.1186/s12915-019-0731-8
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