Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut.
Tsetse flies (Glossina spp.) feed exclusively on vertebrate blood. After a blood meal, the enteric endosymbiont Sodalis glossinidius is exposed to various environmental stressors including high levels of heme. To investigate how S. glossinidius morsitans (Sgm), the Sodalis subspecies that resides wi...
Published in: | PLOS Neglected Tropical Diseases |
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2022
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Online Access: | https://doi.org/10.1371/journal.pntd.0010833 https://doaj.org/article/b83f7d5a57734ba59014683701c52f6b |
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ftdoajarticles:oai:doaj.org/article:b83f7d5a57734ba59014683701c52f6b 2023-05-15T15:14:27+02:00 Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. Laura J Runyen-Janecky Jack D Scheutzow Ruhan Farsin Leah F Cabo Katie E Wall Katrina M Kuhn Rashel Amador Shaina J D'Souza Aurelien Vigneron Brian L Weiss 2022-11-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0010833 https://doaj.org/article/b83f7d5a57734ba59014683701c52f6b EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0010833 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0010833 https://doaj.org/article/b83f7d5a57734ba59014683701c52f6b PLoS Neglected Tropical Diseases, Vol 16, Iss 11, p e0010833 (2022) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2022 ftdoajarticles https://doi.org/10.1371/journal.pntd.0010833 2022-12-30T19:28:45Z Tsetse flies (Glossina spp.) feed exclusively on vertebrate blood. After a blood meal, the enteric endosymbiont Sodalis glossinidius is exposed to various environmental stressors including high levels of heme. To investigate how S. glossinidius morsitans (Sgm), the Sodalis subspecies that resides within the gut of G. morsitans, tolerates the heme-induced oxidative environment of tsetse's midgut, we used RNAseq to identify bacterial genes that are differentially expressed in cells cultured in high versus lower heme environments. Our analysis identified 436 genes that were significantly differentially expressed (> or < 2-fold) in the presence of high heme [219 heme-induced genes (HIGs) and 217 heme-repressed genes (HRGs)]. HIGs were enriched in Gene Ontology (GO) terms related to regulation of a variety of biological functions, including gene expression and metabolic processes. We observed that 11 out of 13 Sgm genes that were heme regulated in vitro were similarly regulated in bacteria that resided within tsetse's midgut 24 hr (high heme environment) and 96 hr (low heme environment) after the flies had consumed a blood meal. We used intron mutagenesis to make insertion mutations in 12 Sgm HIGs and observed no significant change in growth in vitro in any of the mutant strains in high versus low heme conditions. However, Sgm strains that carried mutations in genes encoding a putative undefined phosphotransferase sugar (PTS) system component (SG2427), fucose transporter (SG0182), bacterioferritin (SG2280), and a DNA-binding protein (SGP1-0002), presented growth and/or survival defects in tsetse midguts as compared to normal Sgm. These findings suggest that the uptake up of sugars and storage of iron represent strategies that Sgm employs to successfully reside within the high heme environment of its tsetse host's midgut. Our results are of epidemiological relevance, as many hematophagous arthropods house gut-associated bacteria that mediate their host's competency as a vector of disease-causing pathogens. Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 16 11 e0010833 |
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Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
spellingShingle |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 Laura J Runyen-Janecky Jack D Scheutzow Ruhan Farsin Leah F Cabo Katie E Wall Katrina M Kuhn Rashel Amador Shaina J D'Souza Aurelien Vigneron Brian L Weiss Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
topic_facet |
Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
description |
Tsetse flies (Glossina spp.) feed exclusively on vertebrate blood. After a blood meal, the enteric endosymbiont Sodalis glossinidius is exposed to various environmental stressors including high levels of heme. To investigate how S. glossinidius morsitans (Sgm), the Sodalis subspecies that resides within the gut of G. morsitans, tolerates the heme-induced oxidative environment of tsetse's midgut, we used RNAseq to identify bacterial genes that are differentially expressed in cells cultured in high versus lower heme environments. Our analysis identified 436 genes that were significantly differentially expressed (> or < 2-fold) in the presence of high heme [219 heme-induced genes (HIGs) and 217 heme-repressed genes (HRGs)]. HIGs were enriched in Gene Ontology (GO) terms related to regulation of a variety of biological functions, including gene expression and metabolic processes. We observed that 11 out of 13 Sgm genes that were heme regulated in vitro were similarly regulated in bacteria that resided within tsetse's midgut 24 hr (high heme environment) and 96 hr (low heme environment) after the flies had consumed a blood meal. We used intron mutagenesis to make insertion mutations in 12 Sgm HIGs and observed no significant change in growth in vitro in any of the mutant strains in high versus low heme conditions. However, Sgm strains that carried mutations in genes encoding a putative undefined phosphotransferase sugar (PTS) system component (SG2427), fucose transporter (SG0182), bacterioferritin (SG2280), and a DNA-binding protein (SGP1-0002), presented growth and/or survival defects in tsetse midguts as compared to normal Sgm. These findings suggest that the uptake up of sugars and storage of iron represent strategies that Sgm employs to successfully reside within the high heme environment of its tsetse host's midgut. Our results are of epidemiological relevance, as many hematophagous arthropods house gut-associated bacteria that mediate their host's competency as a vector of disease-causing pathogens. |
format |
Article in Journal/Newspaper |
author |
Laura J Runyen-Janecky Jack D Scheutzow Ruhan Farsin Leah F Cabo Katie E Wall Katrina M Kuhn Rashel Amador Shaina J D'Souza Aurelien Vigneron Brian L Weiss |
author_facet |
Laura J Runyen-Janecky Jack D Scheutzow Ruhan Farsin Leah F Cabo Katie E Wall Katrina M Kuhn Rashel Amador Shaina J D'Souza Aurelien Vigneron Brian L Weiss |
author_sort |
Laura J Runyen-Janecky |
title |
Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
title_short |
Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
title_full |
Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
title_fullStr |
Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
title_full_unstemmed |
Heme-induced genes facilitate endosymbiont (Sodalis glossinidius) colonization of the tsetse fly (Glossina morsitans) midgut. |
title_sort |
heme-induced genes facilitate endosymbiont (sodalis glossinidius) colonization of the tsetse fly (glossina morsitans) midgut. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2022 |
url |
https://doi.org/10.1371/journal.pntd.0010833 https://doaj.org/article/b83f7d5a57734ba59014683701c52f6b |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic |
genre_facet |
Arctic |
op_source |
PLoS Neglected Tropical Diseases, Vol 16, Iss 11, p e0010833 (2022) |
op_relation |
https://doi.org/10.1371/journal.pntd.0010833 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0010833 https://doaj.org/article/b83f7d5a57734ba59014683701c52f6b |
op_doi |
https://doi.org/10.1371/journal.pntd.0010833 |
container_title |
PLOS Neglected Tropical Diseases |
container_volume |
16 |
container_issue |
11 |
container_start_page |
e0010833 |
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1766344904023212032 |