Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum
The microbial community composition of disease vectors can impact pathogen establishment and transmission as well as on vector behavior and fitness. While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely unders...
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| description | The microbial community composition of disease vectors can impact pathogen establishment and transmission as well as on vector behavior and fitness. While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two human-biting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick- and environmentally-related factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology. |
| doi_str_mv | 10.1371/journal.pone.0232398 |
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While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two human-biting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick- and environmentally-related factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0232398</identifier><identifier>PMID: 32413031</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amblyomma americanum ; Arachnids ; Arthropods ; Bacteria ; Biodiversity ; Biology ; Biology and Life Sciences ; Biting ; Borrelia ; Coastal plains ; Community composition ; Composition ; Developmental stages ; Disease transmission ; Diseases ; Ecology and Environmental Sciences ; Encephalitis ; Ethanol ; Females ; Genes ; Hard ticks ; Health aspects ; Identification and classification ; Ixodes scapularis ; Males ; Medicine and Health Sciences ; Microbial activity ; Microbiomes ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Pathogens ; Physiological aspects ; Public health ; Public health movements ; Rickettsia ; RNA ; rRNA 16S ; Sampling ; Species composition ; Species diversity ; Studies ; Taxa ; Tick-borne diseases ; Ticks ; Variation ; Vectors ; Vectors (Biology)</subject><ispartof>PloS one, 2020-05, Vol.15 (5), p.e0232398</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Brinkerhoff et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two human-biting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick- and environmentally-related factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology.</description><subject>Amblyomma americanum</subject><subject>Arachnids</subject><subject>Arthropods</subject><subject>Bacteria</subject><subject>Biodiversity</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Biting</subject><subject>Borrelia</subject><subject>Coastal plains</subject><subject>Community composition</subject><subject>Composition</subject><subject>Developmental stages</subject><subject>Disease transmission</subject><subject>Diseases</subject><subject>Ecology and Environmental Sciences</subject><subject>Encephalitis</subject><subject>Ethanol</subject><subject>Females</subject><subject>Genes</subject><subject>Hard ticks</subject><subject>Health aspects</subject><subject>Identification and classification</subject><subject>Ixodes scapularis</subject><subject>Males</subject><subject>Medicine and Health Sciences</subject><subject>Microbial activity</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Pathogens</subject><subject>Physiological aspects</subject><subject>Public health</subject><subject>Public health movements</subject><subject>Rickettsia</subject><subject>RNA</subject><subject>rRNA 16S</subject><subject>Sampling</subject><subject>Species composition</subject><subject>Species diversity</subject><subject>Studies</subject><subject>Taxa</subject><subject>Tick-borne diseases</subject><subject>Ticks</subject><subject>Variation</subject><subject>Vectors</subject><subject>Vectors 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affecting the microbiome of Ixodes scapularis and Amblyomma americanum</title><author>Brinkerhoff, R Jory ; Clark, Chris ; Ocasio, Kelly ; Gauthier, David T ; Hynes, Wayne L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-f02cf389cf9d1545da7b6722ae81baae2790187134fb1134dfecad4e3aa569c23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amblyomma americanum</topic><topic>Arachnids</topic><topic>Arthropods</topic><topic>Bacteria</topic><topic>Biodiversity</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Biting</topic><topic>Borrelia</topic><topic>Coastal plains</topic><topic>Community composition</topic><topic>Composition</topic><topic>Developmental stages</topic><topic>Disease transmission</topic><topic>Diseases</topic><topic>Ecology and Environmental 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T</au><au>Hynes, Wayne L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-05-15</date><risdate>2020</risdate><volume>15</volume><issue>5</issue><spage>e0232398</spage><pages>e0232398-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The microbial community composition of disease vectors can impact pathogen establishment and transmission as well as on vector behavior and fitness. While data on vector microbiota are accumulating quickly, determinants of the variation in disease vector microbial communities are incompletely understood. We explored the microbiome of two human-biting tick species abundant in eastern North America (Amblyomma americanum and Ixodes scapularis) to identify the relative contribution of tick species, tick life stage, tick sex, environmental context and vertical transmission to the richness, diversity, and species composition of the tick microbiome. We sampled 89 adult and nymphal Ixodes scapularis (N = 49) and Amblyomma americanum (N = 40) from two field sites and characterized the microbiome of each individual using the v3-v4 hypervariable region of the 16S rRNA gene. We identified significant variation in microbial community composition due to tick species and life stage with lesser impact of sampling site. Compared to unfed nymphs and males, the microbiome of engorged adult female I. scapularis, as well as the egg masses they produced, were low in bacterial richness and diversity and were dominated by Rickettsia, suggesting strong vertical transmission of this genus. Likewise, microbiota of A. americanum nymphs and males were more diverse than those of adult females. Among bacteria of public health importance, we detected several different Rickettsia sequence types, several of which were distinct from known species. Borrelia was relatively common in I. scapularis but did not show the same level of sequence variation as Rickettsia. Several bacterial genera were significantly over-represented in Borrelia-infected I. scapularis, suggesting a potential interaction of facilitative relationship between these taxa; no OTUs were under-represented in Borrelia-infected ticks. The systematic sampling we conducted for this study allowed us to partition the variation in tick microbial composition as a function of tick- and environmentally-related factors. Upon more complete understanding of the forces that shape the tick microbiome it will be possible to design targeted experimental studies to test the impacts of individual taxa and suites of microbes on vector-borne pathogen transmission and on vector biology.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32413031</pmid><doi>10.1371/journal.pone.0232398</doi><tpages>e0232398</tpages><orcidid>https://orcid.org/0000-0002-6259-6175</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Amblyomma americanum Arachnids Arthropods Bacteria Biodiversity Biology Biology and Life Sciences Biting Borrelia Coastal plains Community composition Composition Developmental stages Disease transmission Diseases Ecology and Environmental Sciences Encephalitis Ethanol Females Genes Hard ticks Health aspects Identification and classification Ixodes scapularis Males Medicine and Health Sciences Microbial activity Microbiomes Microbiota Microbiota (Symbiotic organisms) Microorganisms Pathogens Physiological aspects Public health Public health movements Rickettsia RNA rRNA 16S Sampling Species composition Species diversity Studies Taxa Tick-borne diseases Ticks Variation Vectors Vectors (Biology) |
| title | Factors affecting the microbiome of Ixodes scapularis and Amblyomma americanum |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T10%3A20%3A03IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Factors%20affecting%20the%20microbiome%20of%20Ixodes%20scapularis%20and%20Amblyomma%20americanum&rft.jtitle=PloS%20one&rft.au=Brinkerhoff,%20R%20Jory&rft.date=2020-05-15&rft.volume=15&rft.issue=5&rft.spage=e0232398&rft.pages=e0232398-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0232398&rft_dat=%3Cgale_plos_%3EA623985309%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2403302513&rft_id=info:pmid/32413031&rft_galeid=A623985309&rft_doaj_id=oai_doaj_org_article_1689053648244e429f9fc6d615a2619d&rfr_iscdi=true |