Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress
In this study, we investigated the global gene expression responses of Elizabethkingia anophelis to iron fluxes in the midgut of female Anopheles stephensi mosquitoes fed sucrose or blood, and in iron-poor or iron-rich culture conditions. Of 3,686 transcripts revealed by RNAseq technology, 218 were...
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Frontiers Media S.A.
2020-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.00804/full |
| _version_ | 1819134464551288832 |
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| author | Shicheng Chen Benjamin K. Johnson Ting Yu Brooke N. Nelson Edward D. Walker Edward D. Walker |
| author_facet | Shicheng Chen Benjamin K. Johnson Ting Yu Brooke N. Nelson Edward D. Walker Edward D. Walker |
| author_sort | Shicheng Chen |
| collection | DOAJ |
| description | In this study, we investigated the global gene expression responses of Elizabethkingia anophelis to iron fluxes in the midgut of female Anopheles stephensi mosquitoes fed sucrose or blood, and in iron-poor or iron-rich culture conditions. Of 3,686 transcripts revealed by RNAseq technology, 218 were upregulated while 112 were down-regulated under iron-poor conditions. Hemolysin gene expression was significantly repressed when cells were grown under iron-rich or high temperature (37°C) conditions. Furthermore, hemolysin gene expression was down-regulated after a blood meal, indicating that E. anophelis cells responded to excess iron and its associated physiological stress by limiting iron loading. By contrast, genes encoding respiratory chain proteins were up-regulated under iron-rich conditions, allowing these iron-containing proteins to chelate intracellular free iron. In vivo studies showed that growth of E. anophelis cells increased 3-fold in blood-fed mosquitoes over those in sucrose-fed ones. Deletion of siderophore synthesis genes led to impaired cell growth in both iron-rich and iron-poor media. Mutants showed more susceptibility to H2O2 toxicity and less biofilm formation than did wild-type cells. Mosquitoes with E. anophelis experimentally colonized in their guts produced more eggs than did those treated with erythromycin or left unmanipulated, as controls. Results reveal that E. anophelis bacteria respond to varying iron concentration in the mosquito gut, harvest iron while fending off iron-associated stress, contribute to lysis of red blood cells, and positively influence mosquito host fecundity. |
| first_indexed | 2024-12-22T10:03:36Z |
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| id | doaj.art-fdf1d4a268b1450397062b61d1e9a25b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-22T10:03:36Z |
| publishDate | 2020-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-fdf1d4a268b1450397062b61d1e9a25b2022-12-21T18:30:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-05-011110.3389/fmicb.2020.00804523247Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron StressShicheng Chen0Benjamin K. Johnson1Ting Yu2Brooke N. Nelson3Edward D. Walker4Edward D. Walker5Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesAgro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, ChinaDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesDepartment of Entomology, Michigan State University, East Lansing, MI, United StatesIn this study, we investigated the global gene expression responses of Elizabethkingia anophelis to iron fluxes in the midgut of female Anopheles stephensi mosquitoes fed sucrose or blood, and in iron-poor or iron-rich culture conditions. Of 3,686 transcripts revealed by RNAseq technology, 218 were upregulated while 112 were down-regulated under iron-poor conditions. Hemolysin gene expression was significantly repressed when cells were grown under iron-rich or high temperature (37°C) conditions. Furthermore, hemolysin gene expression was down-regulated after a blood meal, indicating that E. anophelis cells responded to excess iron and its associated physiological stress by limiting iron loading. By contrast, genes encoding respiratory chain proteins were up-regulated under iron-rich conditions, allowing these iron-containing proteins to chelate intracellular free iron. In vivo studies showed that growth of E. anophelis cells increased 3-fold in blood-fed mosquitoes over those in sucrose-fed ones. Deletion of siderophore synthesis genes led to impaired cell growth in both iron-rich and iron-poor media. Mutants showed more susceptibility to H2O2 toxicity and less biofilm formation than did wild-type cells. Mosquitoes with E. anophelis experimentally colonized in their guts produced more eggs than did those treated with erythromycin or left unmanipulated, as controls. Results reveal that E. anophelis bacteria respond to varying iron concentration in the mosquito gut, harvest iron while fending off iron-associated stress, contribute to lysis of red blood cells, and positively influence mosquito host fecundity.https://www.frontiersin.org/article/10.3389/fmicb.2020.00804/fullElizabethkingiamosquito microbiotairontranscriptomics and geneticsphysiologyoxidative stress |
| spellingShingle | Shicheng Chen Benjamin K. Johnson Ting Yu Brooke N. Nelson Edward D. Walker Edward D. Walker Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress Frontiers in Microbiology Elizabethkingia mosquito microbiota iron transcriptomics and genetics physiology oxidative stress |
| title | Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress |
| title_full | Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress |
| title_fullStr | Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress |
| title_full_unstemmed | Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress |
| title_short | Elizabethkingia anophelis: Physiologic and Transcriptomic Responses to Iron Stress |
| title_sort | elizabethkingia anophelis physiologic and transcriptomic responses to iron stress |
| topic | Elizabethkingia mosquito microbiota iron transcriptomics and genetics physiology oxidative stress |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.00804/full |
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