Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors
Microbial interactions are an underappreciated force in shaping insect microbiome communities. Although pairwise patterns of symbiont interactions have been identified, we have a poor understanding regarding the scale and the nature of co-occurrence and co-exclusion interactions within the microbiom...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-09-01
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| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2018.02160/full |
| _version_ | 1818143969318535168 |
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| author | Shivanand Hegde Kamil Khanipov Kamil Khanipov Levent Albayrak George Golovko Maria Pimenova Miguel A. Saldaña Mark M. Rojas Emily A. Hornett Greg C. Motl Chris L. Fredregill James A. Dennett Mustapha Debboun Yuriy Fofanov Grant L. Hughes |
| author_facet | Shivanand Hegde Kamil Khanipov Kamil Khanipov Levent Albayrak George Golovko Maria Pimenova Miguel A. Saldaña Mark M. Rojas Emily A. Hornett Greg C. Motl Chris L. Fredregill James A. Dennett Mustapha Debboun Yuriy Fofanov Grant L. Hughes |
| author_sort | Shivanand Hegde |
| collection | DOAJ |
| description | Microbial interactions are an underappreciated force in shaping insect microbiome communities. Although pairwise patterns of symbiont interactions have been identified, we have a poor understanding regarding the scale and the nature of co-occurrence and co-exclusion interactions within the microbiome. To characterize these patterns in mosquitoes, we sequenced the bacterial microbiome of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus caught in the field or reared in the laboratory and used these data to generate interaction networks. For collections, we used traps that attracted host-seeking or ovipositing female mosquitoes to determine how physiological state affects the microbiome under field conditions. Interestingly, we saw few differences in species richness or microbiome community structure in mosquitoes caught in either trap. Co-occurrence and co-exclusion analysis identified 116 pairwise interactions substantially increasing the list of bacterial interactions observed in mosquitoes. Networks generated from the microbiome of Ae. aegypti often included highly interconnected hub bacteria. There were several instances where co-occurring bacteria co-excluded a third taxa, suggesting the existence of tripartite relationships. Several associations were observed in multiple species or in field and laboratory-reared mosquitoes indicating these associations are robust and not influenced by environmental or host factors. To demonstrate that microbial interactions can influence colonization of the host, we administered symbionts to Ae. aegypti larvae that either possessed or lacked their resident microbiota. We found that the presence of resident microbiota can inhibit colonization of particular bacterial taxa. Our results highlight that microbial interactions in mosquitoes are complex and influence microbiome composition. |
| first_indexed | 2024-12-11T11:40:07Z |
| format | Article |
| id | doaj.art-906c415e6d12407cadcf5398681d5060 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-11T11:40:07Z |
| publishDate | 2018-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-906c415e6d12407cadcf5398681d50602022-12-22T01:08:37ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-09-01910.3389/fmicb.2018.02160405381Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito VectorsShivanand Hegde0Kamil Khanipov1Kamil Khanipov2Levent Albayrak3George Golovko4Maria Pimenova5Miguel A. Saldaña6Mark M. Rojas7Emily A. Hornett8Greg C. Motl9Chris L. Fredregill10James A. Dennett11Mustapha Debboun12Yuriy Fofanov13Grant L. Hughes14Department of Pathology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology and Molecular Biophysics, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Computer Science, University of Houston, Houston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Zoology, University of Cambridge, Cambridge, United KingdomHarris County Public Health, Mosquito & Vector Control Division, Houston, TX, United StatesHarris County Public Health, Mosquito & Vector Control Division, Houston, TX, United StatesHarris County Public Health, Mosquito & Vector Control Division, Houston, TX, United StatesHarris County Public Health, Mosquito & Vector Control Division, Houston, TX, United StatesDepartment of Pharmacology and Toxicology, Sealy Center for Structural Biology, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Pathology, Institute for Human Infections and Immunity, Center for Tropical Diseases, Center for Biodefense and Emerging Infectious Disease, University of Texas Medical Branch, Galveston, TX, United StatesMicrobial interactions are an underappreciated force in shaping insect microbiome communities. Although pairwise patterns of symbiont interactions have been identified, we have a poor understanding regarding the scale and the nature of co-occurrence and co-exclusion interactions within the microbiome. To characterize these patterns in mosquitoes, we sequenced the bacterial microbiome of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus caught in the field or reared in the laboratory and used these data to generate interaction networks. For collections, we used traps that attracted host-seeking or ovipositing female mosquitoes to determine how physiological state affects the microbiome under field conditions. Interestingly, we saw few differences in species richness or microbiome community structure in mosquitoes caught in either trap. Co-occurrence and co-exclusion analysis identified 116 pairwise interactions substantially increasing the list of bacterial interactions observed in mosquitoes. Networks generated from the microbiome of Ae. aegypti often included highly interconnected hub bacteria. There were several instances where co-occurring bacteria co-excluded a third taxa, suggesting the existence of tripartite relationships. Several associations were observed in multiple species or in field and laboratory-reared mosquitoes indicating these associations are robust and not influenced by environmental or host factors. To demonstrate that microbial interactions can influence colonization of the host, we administered symbionts to Ae. aegypti larvae that either possessed or lacked their resident microbiota. We found that the presence of resident microbiota can inhibit colonization of particular bacterial taxa. Our results highlight that microbial interactions in mosquitoes are complex and influence microbiome composition.https://www.frontiersin.org/article/10.3389/fmicb.2018.02160/fullinteraction networksmicrobe-microbe interactionsgnotobioticgut symbiontgut microbiomeWolbachia |
| spellingShingle | Shivanand Hegde Kamil Khanipov Kamil Khanipov Levent Albayrak George Golovko Maria Pimenova Miguel A. Saldaña Mark M. Rojas Emily A. Hornett Greg C. Motl Chris L. Fredregill James A. Dennett Mustapha Debboun Yuriy Fofanov Grant L. Hughes Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors Frontiers in Microbiology interaction networks microbe-microbe interactions gnotobiotic gut symbiont gut microbiome Wolbachia |
| title | Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors |
| title_full | Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors |
| title_fullStr | Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors |
| title_full_unstemmed | Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors |
| title_short | Microbiome Interaction Networks and Community Structure From Laboratory-Reared and Field-Collected Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus Mosquito Vectors |
| title_sort | microbiome interaction networks and community structure from laboratory reared and field collected aedes aegypti aedes albopictus and culex quinquefasciatus mosquito vectors |
| topic | interaction networks microbe-microbe interactions gnotobiotic gut symbiont gut microbiome Wolbachia |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2018.02160/full |
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