An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea)
Endosymbionts harbored inside insects play critical roles in the biology of their insect host and can influence the transmission of pathogens by insect vectors. <i>Bactericera</i> <i>trigonica</i> infests umbelliferous plants and transmits the bacterial plant pathogen <i&g...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2020-05-01
|
Series: | Microorganisms |
Subjects: | |
Online Access: | https://www.mdpi.com/2076-2607/8/5/692 |
_version_ | 1827717196369887232 |
---|---|
author | Saptarshi Ghosh Noa Sela Svetlana Kontsedalov Galina Lebedev Lee R. Haines Murad Ghanim |
author_facet | Saptarshi Ghosh Noa Sela Svetlana Kontsedalov Galina Lebedev Lee R. Haines Murad Ghanim |
author_sort | Saptarshi Ghosh |
collection | DOAJ |
description | Endosymbionts harbored inside insects play critical roles in the biology of their insect host and can influence the transmission of pathogens by insect vectors. <i>Bactericera</i> <i>trigonica</i> infests umbelliferous plants and transmits the bacterial plant pathogen <i>Candidatus</i> Liberibacter solanacearum (CLso), causing carrot yellows disease. To characterize the bacterial diversity of <i>B. trigonica</i>, as a first step, we used PCR-restriction fragment length polymorphism (PCR-RFLP) and denaturing gradient gel electrophoresis (DGGE) analyses of 16S rDNA to identify <i>Sodalis</i> and <i>Spiroplasma</i> endosymbionts. The prevalence of both symbionts in field-collected psyllid populations was determined: <i>Sodalis</i> was detected in 100% of field populations, while <i>Spiroplasma</i> was present in 82.5% of individuals. Phylogenetic analysis using 16S rDNA revealed that <i>Sodalis</i> infecting <i>B. trigonica</i> was more closely related to symbionts infecting weevils, stink bugs and tsetse flies than to those from psyllid species. Using fluorescent in situ hybridization and immunostaining, <i>Sodalis</i> was found to be localized inside the nuclei of the midgut cells and bacteriocytes. <i>Spiroplasma</i> was restricted to the cytoplasm of the midgut cells. We further show that a recently reported <i>Bactericera trigonica</i> densovirus (BtDNV), a densovirus infecting <i>B. trigonica</i> was detected in 100% of psyllids and has reduced titers inside CLso-infected psyllids by more than two-fold compared to CLso uninfected psyllids. The findings of this study will help to increase our understanding of psyllid–endosymbiont interactions. |
first_indexed | 2024-03-10T19:57:11Z |
format | Article |
id | doaj.art-26b6b48f2ded4ab7af3e45e1f9d87961 |
institution | Directory Open Access Journal |
issn | 2076-2607 |
language | English |
last_indexed | 2024-03-10T19:57:11Z |
publishDate | 2020-05-01 |
publisher | MDPI AG |
record_format | Article |
series | Microorganisms |
spelling | doaj.art-26b6b48f2ded4ab7af3e45e1f9d879612023-11-19T23:51:29ZengMDPI AGMicroorganisms2076-26072020-05-018569210.3390/microorganisms8050692An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea)Saptarshi Ghosh0Noa Sela1Svetlana Kontsedalov2Galina Lebedev3Lee R. Haines4Murad Ghanim5Department of Entomology, Institute of Plant Protection, Volcani Center, ARO, HaMaccabim Road 68, P.O. Box 15159, Rishon LeZion 7528809, IsraelDepartment of Plant Pathology and Weed Research, Institute of Plant Protection, Volcani Center, ARO, HaMaccabim Road 68, P.O. Box 15159, Rishon LeZion 7528809, IsraelDepartment of Entomology, Institute of Plant Protection, Volcani Center, ARO, HaMaccabim Road 68, P.O. Box 15159, Rishon LeZion 7528809, IsraelDepartment of Entomology, Institute of Plant Protection, Volcani Center, ARO, HaMaccabim Road 68, P.O. Box 15159, Rishon LeZion 7528809, IsraelDepartment of Vector Biology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UKDepartment of Entomology, Institute of Plant Protection, Volcani Center, ARO, HaMaccabim Road 68, P.O. Box 15159, Rishon LeZion 7528809, IsraelEndosymbionts harbored inside insects play critical roles in the biology of their insect host and can influence the transmission of pathogens by insect vectors. <i>Bactericera</i> <i>trigonica</i> infests umbelliferous plants and transmits the bacterial plant pathogen <i>Candidatus</i> Liberibacter solanacearum (CLso), causing carrot yellows disease. To characterize the bacterial diversity of <i>B. trigonica</i>, as a first step, we used PCR-restriction fragment length polymorphism (PCR-RFLP) and denaturing gradient gel electrophoresis (DGGE) analyses of 16S rDNA to identify <i>Sodalis</i> and <i>Spiroplasma</i> endosymbionts. The prevalence of both symbionts in field-collected psyllid populations was determined: <i>Sodalis</i> was detected in 100% of field populations, while <i>Spiroplasma</i> was present in 82.5% of individuals. Phylogenetic analysis using 16S rDNA revealed that <i>Sodalis</i> infecting <i>B. trigonica</i> was more closely related to symbionts infecting weevils, stink bugs and tsetse flies than to those from psyllid species. Using fluorescent in situ hybridization and immunostaining, <i>Sodalis</i> was found to be localized inside the nuclei of the midgut cells and bacteriocytes. <i>Spiroplasma</i> was restricted to the cytoplasm of the midgut cells. We further show that a recently reported <i>Bactericera trigonica</i> densovirus (BtDNV), a densovirus infecting <i>B. trigonica</i> was detected in 100% of psyllids and has reduced titers inside CLso-infected psyllids by more than two-fold compared to CLso uninfected psyllids. The findings of this study will help to increase our understanding of psyllid–endosymbiont interactions.https://www.mdpi.com/2076-2607/8/5/692psyllid<i>Bactericera trigonica</i><i>Candidatus</i> Liberibacter solanacearumsecondary endosymbiont<i>Sodalis</i><i>Spiroplasma</i> |
spellingShingle | Saptarshi Ghosh Noa Sela Svetlana Kontsedalov Galina Lebedev Lee R. Haines Murad Ghanim An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) Microorganisms psyllid <i>Bactericera trigonica</i> <i>Candidatus</i> Liberibacter solanacearum secondary endosymbiont <i>Sodalis</i> <i>Spiroplasma</i> |
title | An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) |
title_full | An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) |
title_fullStr | An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) |
title_full_unstemmed | An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) |
title_short | An Intranuclear <i>Sodalis</i>-Like Symbiont and <i>Spiroplasma</i> Coinfect the Carrot Psyllid, <i>Bactericera trigonica</i> (Hemiptera, Psylloidea) |
title_sort | intranuclear i sodalis i like symbiont and i spiroplasma i coinfect the carrot psyllid i bactericera trigonica i hemiptera psylloidea |
topic | psyllid <i>Bactericera trigonica</i> <i>Candidatus</i> Liberibacter solanacearum secondary endosymbiont <i>Sodalis</i> <i>Spiroplasma</i> |
url | https://www.mdpi.com/2076-2607/8/5/692 |
work_keys_str_mv | AT saptarshighosh anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT noasela anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT svetlanakontsedalov anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT galinalebedev anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT leerhaines anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT muradghanim anintranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT saptarshighosh intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT noasela intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT svetlanakontsedalov intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT galinalebedev intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT leerhaines intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea AT muradghanim intranuclearisodalisilikesymbiontandispiroplasmaicoinfectthecarrotpsyllidibactericeratrigonicaihemipterapsylloidea |