A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world

Abstract It is currently assumed that around 100 million years ago, the common ancestor to the Fabales, Fagales, Rosales and Cucurbitales in Gondwana, developed a root nodule symbiosis with a nitrogen-fixing bacterium. The symbiotic trait evolved first in Frankia cluster-2; thus, strains belonging t...

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Main Authors: Fede Berckx, Thanh Van Nguyen, Cyndi Mae Bandong, Hsiao-Han Lin, Takashi Yamanaka, Sae Katayama, Daniel Wibberg, Jochen Blom, Jörn Kalinowski, Masaki Tateno, Jessica Simbahan, Chi-Te Liu, Andreas Brachmann, Katharina Pawlowski
Format: Article
Language:English
Published: BMC 2022-08-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-022-08838-5
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author Fede Berckx
Thanh Van Nguyen
Cyndi Mae Bandong
Hsiao-Han Lin
Takashi Yamanaka
Sae Katayama
Daniel Wibberg
Jochen Blom
Jörn Kalinowski
Masaki Tateno
Jessica Simbahan
Chi-Te Liu
Andreas Brachmann
Katharina Pawlowski
author_facet Fede Berckx
Thanh Van Nguyen
Cyndi Mae Bandong
Hsiao-Han Lin
Takashi Yamanaka
Sae Katayama
Daniel Wibberg
Jochen Blom
Jörn Kalinowski
Masaki Tateno
Jessica Simbahan
Chi-Te Liu
Andreas Brachmann
Katharina Pawlowski
author_sort Fede Berckx
collection DOAJ
description Abstract It is currently assumed that around 100 million years ago, the common ancestor to the Fabales, Fagales, Rosales and Cucurbitales in Gondwana, developed a root nodule symbiosis with a nitrogen-fixing bacterium. The symbiotic trait evolved first in Frankia cluster-2; thus, strains belonging to this cluster are the best extant representatives of this original symbiont. Most cluster-2 strains could not be cultured to date, except for Frankia coriariae, and therefore many aspects of the symbiosis are still elusive. Based on phylogenetics of cluster-2 metagenome-assembled genomes (MAGs), it has been shown that the genomes of strains originating in Eurasia are highly conserved. These MAGs are more closely related to Frankia cluster-2 in North America than to the single genome available thus far from the southern hemisphere, i.e., from Papua New Guinea. To unravel more biodiversity within Frankia cluster-2 and predict routes of dispersal from Gondwana, we sequenced and analysed the MAGs of Frankia cluster-2 from Coriaria japonica and Coriaria intermedia growing in Japan, Taiwan and the Philippines. Phylogenetic analyses indicate there is a clear split within Frankia cluster-2, separating a continental from an island lineage. Presumably, these lineages already diverged in Gondwana. Based on fossil data on the host plants, we propose that these two lineages dispersed via at least two routes. While the continental lineage reached Eurasia together with their host plants via the Indian subcontinent, the island lineage spread towards Japan with an unknown host plant.
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spelling doaj.art-b8dd3cdf056d45daa7d87580416d71812022-12-22T02:34:51ZengBMCBMC Genomics1471-21642022-08-0123111210.1186/s12864-022-08838-5A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the worldFede Berckx0Thanh Van Nguyen1Cyndi Mae Bandong2Hsiao-Han Lin3Takashi Yamanaka4Sae Katayama5Daniel Wibberg6Jochen Blom7Jörn Kalinowski8Masaki Tateno9Jessica Simbahan10Chi-Te Liu11Andreas Brachmann12Katharina Pawlowski13Department of Ecology, Environment and Plant SciencesDepartment of Ecology, Environment and Plant SciencesDepartment of Ecology, Environment and Plant SciencesInstitute of Biotechnology, National Taiwan UniversityForest Research and Management OrganizationNikko Botanical Garden, Department of Biological Sciences, Graduate School of Science, The University of TokyoCenter for Biotechnology (CeBiTec), Bielefeld UniversityBioinformatics and Systems Biology, Justus Liebig UniversityCenter for Biotechnology (CeBiTec), Bielefeld UniversityNikko Botanical Garden, Department of Biological Sciences, Graduate School of Science, The University of TokyoCollege of Science, University of the PhilippinesInstitute of Biotechnology, National Taiwan UniversityBiocenter, LMU MünchenDepartment of Ecology, Environment and Plant SciencesAbstract It is currently assumed that around 100 million years ago, the common ancestor to the Fabales, Fagales, Rosales and Cucurbitales in Gondwana, developed a root nodule symbiosis with a nitrogen-fixing bacterium. The symbiotic trait evolved first in Frankia cluster-2; thus, strains belonging to this cluster are the best extant representatives of this original symbiont. Most cluster-2 strains could not be cultured to date, except for Frankia coriariae, and therefore many aspects of the symbiosis are still elusive. Based on phylogenetics of cluster-2 metagenome-assembled genomes (MAGs), it has been shown that the genomes of strains originating in Eurasia are highly conserved. These MAGs are more closely related to Frankia cluster-2 in North America than to the single genome available thus far from the southern hemisphere, i.e., from Papua New Guinea. To unravel more biodiversity within Frankia cluster-2 and predict routes of dispersal from Gondwana, we sequenced and analysed the MAGs of Frankia cluster-2 from Coriaria japonica and Coriaria intermedia growing in Japan, Taiwan and the Philippines. Phylogenetic analyses indicate there is a clear split within Frankia cluster-2, separating a continental from an island lineage. Presumably, these lineages already diverged in Gondwana. Based on fossil data on the host plants, we propose that these two lineages dispersed via at least two routes. While the continental lineage reached Eurasia together with their host plants via the Indian subcontinent, the island lineage spread towards Japan with an unknown host plant.https://doi.org/10.1186/s12864-022-08838-5Root nodulesFrankiaCoriariaActinorhizal symbiosisBiogeography
spellingShingle Fede Berckx
Thanh Van Nguyen
Cyndi Mae Bandong
Hsiao-Han Lin
Takashi Yamanaka
Sae Katayama
Daniel Wibberg
Jochen Blom
Jörn Kalinowski
Masaki Tateno
Jessica Simbahan
Chi-Te Liu
Andreas Brachmann
Katharina Pawlowski
A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
BMC Genomics
Root nodules
Frankia
Coriaria
Actinorhizal symbiosis
Biogeography
title A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
title_full A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
title_fullStr A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
title_full_unstemmed A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
title_short A tale of two lineages: how the strains of the earliest divergent symbiotic Frankia clade spread over the world
title_sort tale of two lineages how the strains of the earliest divergent symbiotic frankia clade spread over the world
topic Root nodules
Frankia
Coriaria
Actinorhizal symbiosis
Biogeography
url https://doi.org/10.1186/s12864-022-08838-5
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