Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes

Bacteria of the genus “<i>Candidatus</i> Cardinium” and related organisms composing the <i>Cardinium</i> clade are intracellular endosymbionts frequently occurring in several arthropod groups, freshwater mussels and plant-parasitic nematodes. Phylogenetic analyses based on tw...

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Main Authors: Sergey V. Tarlachkov, Boris D. Efeykin, Pablo Castillo, Lyudmila I. Evtushenko, Sergei A. Subbotin
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/3/2905
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author Sergey V. Tarlachkov
Boris D. Efeykin
Pablo Castillo
Lyudmila I. Evtushenko
Sergei A. Subbotin
author_facet Sergey V. Tarlachkov
Boris D. Efeykin
Pablo Castillo
Lyudmila I. Evtushenko
Sergei A. Subbotin
author_sort Sergey V. Tarlachkov
collection DOAJ
description Bacteria of the genus “<i>Candidatus</i> Cardinium” and related organisms composing the <i>Cardinium</i> clade are intracellular endosymbionts frequently occurring in several arthropod groups, freshwater mussels and plant-parasitic nematodes. Phylogenetic analyses based on two gene sequences (16S rRNA and <i>gyrB</i>) showed that the <i>Cardinium</i> clade comprised at least five groups: A, B, C, D and E. In this study, a screening of 142 samples of plant-parasitic nematodes belonging to 93 species from 12 families and two orders using PCR with specific primers and sequencing, revealed bacteria of <i>Cardinium</i> clade in 14 nematode samples belonging to 12 species of cyst nematodes of the family Heteroderidae. Furthermore, in this study, the genome of the <i>Cardinium</i> cHhum from the hop cyst nematode, <i>Heterodera humuli,</i> was also amplified, sequenced and analyzed. The comparisons of the average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) values for the strain <i>Cardinium</i> cHhum with regard to related organisms with available genomes, combined with the data on 16S rRNA and <i>gyrB</i> gene sequence identities, showed that this strain represents a new candidate species within the genus “<i>Candidatus</i> Paenicardinium”. The phylogenetic position of endosymbionts of the <i>Cardinium</i> clade detected in nematode hosts was also compared to known representatives of this clade from other metazoans. Phylogenetic reconstructions based on analysis of 16S rRNA, <i>gyrB, sufB, gloEL, fusA, infB</i> genes and genomes and estimates of genetic distances both indicate that the endosymbiont of the root-lesion nematode <i>Pratylenchus penetrans</i> represented a separate lineage and is designated herein as a new group F. The phylogenetic analysis also confirmed that endosymbionts of ostracods represent the novel group G. Evolutionary relationships of bacterial endosymbionts of the <i>Cardinium</i> clade within invertebrates are presented and discussed.
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spelling doaj.art-99460200f888427c9ccd578306955dba2023-11-16T17:04:11ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-02-01243290510.3390/ijms24032905Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic NematodesSergey V. Tarlachkov0Boris D. Efeykin1Pablo Castillo2Lyudmila I. Evtushenko3Sergei A. Subbotin4All-Russian Collection of Microorganisms (VKM), G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences, Pushchino 142290, RussiaCenter of Parasitology of A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskii Prospect 33, Moscow 117071, RussiaInstitute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Avenida Menéndez Pidal s/n, Campus de Excelencia Internacional Agroalimentario, ceiA3, 14004 Córdoba, SpainAll-Russian Collection of Microorganisms (VKM), G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences, Pushchino 142290, RussiaCenter of Parasitology of A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninskii Prospect 33, Moscow 117071, RussiaBacteria of the genus “<i>Candidatus</i> Cardinium” and related organisms composing the <i>Cardinium</i> clade are intracellular endosymbionts frequently occurring in several arthropod groups, freshwater mussels and plant-parasitic nematodes. Phylogenetic analyses based on two gene sequences (16S rRNA and <i>gyrB</i>) showed that the <i>Cardinium</i> clade comprised at least five groups: A, B, C, D and E. In this study, a screening of 142 samples of plant-parasitic nematodes belonging to 93 species from 12 families and two orders using PCR with specific primers and sequencing, revealed bacteria of <i>Cardinium</i> clade in 14 nematode samples belonging to 12 species of cyst nematodes of the family Heteroderidae. Furthermore, in this study, the genome of the <i>Cardinium</i> cHhum from the hop cyst nematode, <i>Heterodera humuli,</i> was also amplified, sequenced and analyzed. The comparisons of the average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) values for the strain <i>Cardinium</i> cHhum with regard to related organisms with available genomes, combined with the data on 16S rRNA and <i>gyrB</i> gene sequence identities, showed that this strain represents a new candidate species within the genus “<i>Candidatus</i> Paenicardinium”. The phylogenetic position of endosymbionts of the <i>Cardinium</i> clade detected in nematode hosts was also compared to known representatives of this clade from other metazoans. Phylogenetic reconstructions based on analysis of 16S rRNA, <i>gyrB, sufB, gloEL, fusA, infB</i> genes and genomes and estimates of genetic distances both indicate that the endosymbiont of the root-lesion nematode <i>Pratylenchus penetrans</i> represented a separate lineage and is designated herein as a new group F. The phylogenetic analysis also confirmed that endosymbionts of ostracods represent the novel group G. Evolutionary relationships of bacterial endosymbionts of the <i>Cardinium</i> clade within invertebrates are presented and discussed.https://www.mdpi.com/1422-0067/24/3/2905<i>Cardinium</i>genomenematodenovel group<i>Paenicardinium</i>phylogeny
spellingShingle Sergey V. Tarlachkov
Boris D. Efeykin
Pablo Castillo
Lyudmila I. Evtushenko
Sergei A. Subbotin
Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
International Journal of Molecular Sciences
<i>Cardinium</i>
genome
nematode
novel group
<i>Paenicardinium</i>
phylogeny
title Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
title_full Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
title_fullStr Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
title_full_unstemmed Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
title_short Distribution of Bacterial Endosymbionts of the <i>Cardinium</i> Clade in Plant-Parasitic Nematodes
title_sort distribution of bacterial endosymbionts of the i cardinium i clade in plant parasitic nematodes
topic <i>Cardinium</i>
genome
nematode
novel group
<i>Paenicardinium</i>
phylogeny
url https://www.mdpi.com/1422-0067/24/3/2905
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