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Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips

Awawing Anjwengwo Andongma, MIRANDA WHITTEN, Ricardo Del Sol Abascal Orcid Logo, Matthew Hitchings Orcid Logo, Paul Dyson Orcid Logo

Frontiers in Microbiology, Volume: 13

Swansea University Authors: Awawing Anjwengwo Andongma, MIRANDA WHITTEN, Ricardo Del Sol Abascal Orcid Logo, Matthew Hitchings Orcid Logo, Paul Dyson Orcid Logo

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DOI (Published version): 10.3389/fmicb.2022.883891

Abstract

Symbiont mediated RNAi (SMR) is a promising method for precision control of pest insect species such as Western Flower Thrips (WFT). Two species of bacteria are known to be dominant symbiotic bacteria in WFT, namely BFo1 and BFo2 (Bacteria from Frankliniella occidentalis 1 and 2), as we here confirm...

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Published in: Frontiers in Microbiology
ISSN: 1664-302X
Published: Frontiers Media SA 2022
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Two species of bacteria are known to be dominant symbiotic bacteria in WFT, namely BFo1 and BFo2 (Bacteria from Frankliniella occidentalis 1 and 2), as we here confirm by analysis of next-generation sequence data derived to obtain a reference WFT genome sequence. Our first demonstration of SMR in WFT used BFo2, related to Pantoea, isolated from a domesticated Dutch thrips population. However, for successful use of SMR as a thrips control measure, these bacteria need to successfully colonize different environmental thrips populations. Here, we describe a United Kingdom thrips population that does not harbour BFo2, but does contain BFo1, a species related to Erwinia. Attempts to introduce BFo2 indicate that this bacterium is unable to establish itself in the United Kingdom thrips, in contrast to successful colonization by a strain of BFo1 expressing green fluorescent protein. Fluorescence microscopy indicates that BFo1 occupies similar regions of the thrips posterior midgut and hindgut as BFo2. Bacterial competition assays revealed that a barrier to BFo2 establishing itself in thrips is the identity of the resident BFo1; BFo1 isolated from the United Kingdom thrips suppresses growth of BFo2 to a greater extent than BFo1 from the Dutch thrips that is permissive for BFo2 colonization. The ability of the latter strain of BFo1 to colonize the United Kingdom thrips is also likely attributable to its ability to out-compete the resident BFo1. Lastly, we observed that United Kingdom thrips pre-exposed to the Dutch BFo1 could then be successfully colonized by BFo2. These results indicate, for the first time, that microbial competition and strain differences can have a large influence on how symbiotic bacteria can colonize different populations of an insect species.</abstract><type>Journal Article</type><journal>Frontiers in Microbiology</journal><volume>13</volume><journalNumber/><paginationStart/><paginationEnd/><publisher>Frontiers Media SA</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>1664-302X</issnElectronic><keywords>Western Flower Thrips; bacterial competition; next-generation sequencing; paratransgenesis; symbiotic bacteria.</keywords><publishedDay>7</publishedDay><publishedMonth>7</publishedMonth><publishedYear>2022</publishedYear><publishedDate>2022-07-07</publishedDate><doi>10.3389/fmicb.2022.883891</doi><url>http://dx.doi.org/10.3389/fmicb.2022.883891</url><notes/><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm>External research funder(s) paid the OA fee (includes OA grants disbursed by the Library)</apcterm><funders>UKRI (BBSRC grant ref. 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spelling 2022-08-10T17:00:27.6270177 v2 60193 2022-06-13 Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips 6d83c753a85242a9fb9a366ab5636d69 Awawing Anjwengwo Andongma Awawing Anjwengwo Andongma true false 8cfc6fba1ff5757e497fa4d542733559 MIRANDA WHITTEN MIRANDA WHITTEN true false c40efdd0f744eef81f726c98cec03d07 0000-0003-0015-3843 Ricardo Del Sol Abascal Ricardo Del Sol Abascal true false be98847c72c14a731c4a6b7bc02b3bcf 0000-0002-5527-4709 Matthew Hitchings Matthew Hitchings true false 300e3f46b70ae83f563b24f41d00cd17 0000-0002-0558-2666 Paul Dyson Paul Dyson true false 2022-06-13 BMS Symbiont mediated RNAi (SMR) is a promising method for precision control of pest insect species such as Western Flower Thrips (WFT). Two species of bacteria are known to be dominant symbiotic bacteria in WFT, namely BFo1 and BFo2 (Bacteria from Frankliniella occidentalis 1 and 2), as we here confirm by analysis of next-generation sequence data derived to obtain a reference WFT genome sequence. Our first demonstration of SMR in WFT used BFo2, related to Pantoea, isolated from a domesticated Dutch thrips population. However, for successful use of SMR as a thrips control measure, these bacteria need to successfully colonize different environmental thrips populations. Here, we describe a United Kingdom thrips population that does not harbour BFo2, but does contain BFo1, a species related to Erwinia. Attempts to introduce BFo2 indicate that this bacterium is unable to establish itself in the United Kingdom thrips, in contrast to successful colonization by a strain of BFo1 expressing green fluorescent protein. Fluorescence microscopy indicates that BFo1 occupies similar regions of the thrips posterior midgut and hindgut as BFo2. Bacterial competition assays revealed that a barrier to BFo2 establishing itself in thrips is the identity of the resident BFo1; BFo1 isolated from the United Kingdom thrips suppresses growth of BFo2 to a greater extent than BFo1 from the Dutch thrips that is permissive for BFo2 colonization. The ability of the latter strain of BFo1 to colonize the United Kingdom thrips is also likely attributable to its ability to out-compete the resident BFo1. Lastly, we observed that United Kingdom thrips pre-exposed to the Dutch BFo1 could then be successfully colonized by BFo2. These results indicate, for the first time, that microbial competition and strain differences can have a large influence on how symbiotic bacteria can colonize different populations of an insect species. Journal Article Frontiers in Microbiology 13 Frontiers Media SA 1664-302X Western Flower Thrips; bacterial competition; next-generation sequencing; paratransgenesis; symbiotic bacteria. 7 7 2022 2022-07-07 10.3389/fmicb.2022.883891 http://dx.doi.org/10.3389/fmicb.2022.883891 COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University External research funder(s) paid the OA fee (includes OA grants disbursed by the Library) UKRI (BBSRC grant ref. BB/R006148/1) to PD. We also acknowledge the support of the Supercomputing Wales project, which is part-funded by the European Regional Development Fund (ERDF) via Welsh Government. BB/R006148/1 2022-08-10T17:00:27.6270177 2022-06-13T18:15:23.8439238 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Awawing Anjwengwo Andongma 1 MIRANDA WHITTEN 2 Ricardo Del Sol Abascal 0000-0003-0015-3843 3 Matthew Hitchings 0000-0002-5527-4709 4 Paul Dyson 0000-0002-0558-2666 5 60193__24907__89ecc7681b1441658632db7d548af8c1.pdf 60193.VOR.pdf 2022-08-10T16:53:57.7435342 Output 1819276 application/pdf Version of Record true Distributed under the terms of a Creative Commons Attribution 4.0 CC-BY License. true eng http://creativecommons.org/licenses/by/4.0/
title Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
spellingShingle Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
Awawing Anjwengwo Andongma
MIRANDA WHITTEN
Ricardo Del Sol Abascal
Matthew Hitchings
Paul Dyson
title_short Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
title_full Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
title_fullStr Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
title_full_unstemmed Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
title_sort Bacterial Competition Influences the Ability of Symbiotic Bacteria to Colonize Western Flower Thrips
author_id_str_mv 6d83c753a85242a9fb9a366ab5636d69
8cfc6fba1ff5757e497fa4d542733559
c40efdd0f744eef81f726c98cec03d07
be98847c72c14a731c4a6b7bc02b3bcf
300e3f46b70ae83f563b24f41d00cd17
author_id_fullname_str_mv 6d83c753a85242a9fb9a366ab5636d69_***_Awawing Anjwengwo Andongma
8cfc6fba1ff5757e497fa4d542733559_***_MIRANDA WHITTEN
c40efdd0f744eef81f726c98cec03d07_***_Ricardo Del Sol Abascal
be98847c72c14a731c4a6b7bc02b3bcf_***_Matthew Hitchings
300e3f46b70ae83f563b24f41d00cd17_***_Paul Dyson
author Awawing Anjwengwo Andongma
MIRANDA WHITTEN
Ricardo Del Sol Abascal
Matthew Hitchings
Paul Dyson
author2 Awawing Anjwengwo Andongma
MIRANDA WHITTEN
Ricardo Del Sol Abascal
Matthew Hitchings
Paul Dyson
format Journal article
container_title Frontiers in Microbiology
container_volume 13
publishDate 2022
institution Swansea University
issn 1664-302X
doi_str_mv 10.3389/fmicb.2022.883891
publisher Frontiers Media SA
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
url http://dx.doi.org/10.3389/fmicb.2022.883891
document_store_str 1
active_str 0
description Symbiont mediated RNAi (SMR) is a promising method for precision control of pest insect species such as Western Flower Thrips (WFT). Two species of bacteria are known to be dominant symbiotic bacteria in WFT, namely BFo1 and BFo2 (Bacteria from Frankliniella occidentalis 1 and 2), as we here confirm by analysis of next-generation sequence data derived to obtain a reference WFT genome sequence. Our first demonstration of SMR in WFT used BFo2, related to Pantoea, isolated from a domesticated Dutch thrips population. However, for successful use of SMR as a thrips control measure, these bacteria need to successfully colonize different environmental thrips populations. Here, we describe a United Kingdom thrips population that does not harbour BFo2, but does contain BFo1, a species related to Erwinia. Attempts to introduce BFo2 indicate that this bacterium is unable to establish itself in the United Kingdom thrips, in contrast to successful colonization by a strain of BFo1 expressing green fluorescent protein. Fluorescence microscopy indicates that BFo1 occupies similar regions of the thrips posterior midgut and hindgut as BFo2. Bacterial competition assays revealed that a barrier to BFo2 establishing itself in thrips is the identity of the resident BFo1; BFo1 isolated from the United Kingdom thrips suppresses growth of BFo2 to a greater extent than BFo1 from the Dutch thrips that is permissive for BFo2 colonization. The ability of the latter strain of BFo1 to colonize the United Kingdom thrips is also likely attributable to its ability to out-compete the resident BFo1. Lastly, we observed that United Kingdom thrips pre-exposed to the Dutch BFo1 could then be successfully colonized by BFo2. These results indicate, for the first time, that microbial competition and strain differences can have a large influence on how symbiotic bacteria can colonize different populations of an insect species.
published_date 2022-07-07T04:18:06Z
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