Toll receptor ligand Spätzle 4 responses to the highly pathogenic Enterococcus faecalis from Varroa mites in honeybees
Honeybees play a major role in crop pollination, which supports the agricultural economy and international food supply. The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Rec...
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description | Honeybees play a major role in crop pollination, which supports the agricultural economy and international food supply. The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Recently, it shows that V. destructor may also transmit bacteria through the feeding wound, yet it remains unclear whether the invading bacteria can exhibit pathogenicity to the honeybees. Here, we incidentally isolate Enterococcus faecalis, one of the most abundant bacteria in Varroa mites, from dead bees during our routine generation of microbiota-free bees in the lab. In vivo tests show that E. faecalis is only pathogenic in Apis mellifera but not in Apis cerana. The expression of antimicrobial peptide genes is elevated following infection in A. cerana. The gene-based molecular evolution analysis identifies positive selection of genes encoding Späetzle 4 (Spz4) in A. cerana, a signaling protein in the Toll pathway. The amino acid sites under positive selection are related to structural changes in Spz4 protein, suggesting improvement of immunity in A. cerana. The knock-down of Spz4 in A. cerana significantly reduces the survival rates under E. faecalis challenge and the expression of antimicrobial peptide genes. Our results indicate that bacteria associated with Varroa mites are pathogenic to adult bees, and the positively selected gene Spz4 in A. cerana is crucial in response to this mite-related pathogen. |
doi_str_mv | 10.1371/journal.ppat.1011897 |
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The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Recently, it shows that V. destructor may also transmit bacteria through the feeding wound, yet it remains unclear whether the invading bacteria can exhibit pathogenicity to the honeybees. Here, we incidentally isolate Enterococcus faecalis, one of the most abundant bacteria in Varroa mites, from dead bees during our routine generation of microbiota-free bees in the lab. In vivo tests show that E. faecalis is only pathogenic in Apis mellifera but not in Apis cerana. The expression of antimicrobial peptide genes is elevated following infection in A. cerana. The gene-based molecular evolution analysis identifies positive selection of genes encoding Späetzle 4 (Spz4) in A. cerana, a signaling protein in the Toll pathway. The amino acid sites under positive selection are related to structural changes in Spz4 protein, suggesting improvement of immunity in A. cerana. The knock-down of Spz4 in A. cerana significantly reduces the survival rates under E. faecalis challenge and the expression of antimicrobial peptide genes. Our results indicate that bacteria associated with Varroa mites are pathogenic to adult bees, and the positively selected gene Spz4 in A. cerana is crucial in response to this mite-related pathogen.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1011897</identifier><identifier>PMID: 38150483</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acids ; Analysis ; Animals ; Antimicrobial Peptides ; Apis mellifera ; Bacteria ; Bees ; Biology and Life Sciences ; Casualties ; Composition ; Control ; Diseases ; Enterococcal infections ; Enterococcus faecalis ; Enterococcus faecalis - genetics ; Evolutionary genetics ; Food ; Food supply ; Gene expression ; Genes ; Genetic aspects ; Genetic vectors ; Genomes ; Growth ; Health aspects ; Honeybee ; In vivo methods and tests ; Infections ; Ligands ; Medicine and Health Sciences ; Microbiota ; Microbiota (Symbiotic organisms) ; Mites ; Molecular evolution ; Mortality ; Pathogenicity ; Pathogens ; Pollination ; Positive selection ; Prevention ; Proteins ; Risk factors ; Sucrose ; Survival ; Varroa destructor ; Varroidae - physiology ; Virulence</subject><ispartof>PLoS pathogens, 2023-12, Vol.19 (12), p.e1011897-e1011897</ispartof><rights>Copyright: © 2023 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Zhang 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Zhang et al 2023 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c611t-f65c1b07f67453943ad36898dcfe391873f95178a56cd4d1d21d19b86a564eb53</cites><orcidid>0000-0002-6446-5486 ; 0000-0003-3313-1675</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10775982/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10775982/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38150483$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Wenhao</creatorcontrib><creatorcontrib>Sun, Cheng</creatorcontrib><creatorcontrib>Lang, Haoyu</creatorcontrib><creatorcontrib>Wang, Jieni</creatorcontrib><creatorcontrib>Li, Xinyu</creatorcontrib><creatorcontrib>Guo, Jun</creatorcontrib><creatorcontrib>Zhang, Zijing</creatorcontrib><creatorcontrib>Zheng, Hao</creatorcontrib><title>Toll receptor ligand Spätzle 4 responses to the highly pathogenic Enterococcus faecalis from Varroa mites in honeybees</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Honeybees play a major role in crop pollination, which supports the agricultural economy and international food supply. The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Recently, it shows that V. destructor may also transmit bacteria through the feeding wound, yet it remains unclear whether the invading bacteria can exhibit pathogenicity to the honeybees. Here, we incidentally isolate Enterococcus faecalis, one of the most abundant bacteria in Varroa mites, from dead bees during our routine generation of microbiota-free bees in the lab. In vivo tests show that E. faecalis is only pathogenic in Apis mellifera but not in Apis cerana. The expression of antimicrobial peptide genes is elevated following infection in A. cerana. The gene-based molecular evolution analysis identifies positive selection of genes encoding Späetzle 4 (Spz4) in A. cerana, a signaling protein in the Toll pathway. The amino acid sites under positive selection are related to structural changes in Spz4 protein, suggesting improvement of immunity in A. cerana. The knock-down of Spz4 in A. cerana significantly reduces the survival rates under E. faecalis challenge and the expression of antimicrobial peptide genes. Our results indicate that bacteria associated with Varroa mites are pathogenic to adult bees, and the positively selected gene Spz4 in A. cerana is crucial in response to this mite-related pathogen.</description><subject>Amino acids</subject><subject>Analysis</subject><subject>Animals</subject><subject>Antimicrobial Peptides</subject><subject>Apis mellifera</subject><subject>Bacteria</subject><subject>Bees</subject><subject>Biology and Life Sciences</subject><subject>Casualties</subject><subject>Composition</subject><subject>Control</subject><subject>Diseases</subject><subject>Enterococcal infections</subject><subject>Enterococcus faecalis</subject><subject>Enterococcus faecalis - genetics</subject><subject>Evolutionary genetics</subject><subject>Food</subject><subject>Food supply</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic vectors</subject><subject>Genomes</subject><subject>Growth</subject><subject>Health aspects</subject><subject>Honeybee</subject><subject>In vivo methods and tests</subject><subject>Infections</subject><subject>Ligands</subject><subject>Medicine and Health Sciences</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Mites</subject><subject>Molecular evolution</subject><subject>Mortality</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Pollination</subject><subject>Positive selection</subject><subject>Prevention</subject><subject>Proteins</subject><subject>Risk factors</subject><subject>Sucrose</subject><subject>Survival</subject><subject>Varroa destructor</subject><subject>Varroidae - 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genetics</topic><topic>Evolutionary genetics</topic><topic>Food</topic><topic>Food supply</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic vectors</topic><topic>Genomes</topic><topic>Growth</topic><topic>Health aspects</topic><topic>Honeybee</topic><topic>In vivo methods and tests</topic><topic>Infections</topic><topic>Ligands</topic><topic>Medicine and Health Sciences</topic><topic>Microbiota</topic><topic>Microbiota (Symbiotic organisms)</topic><topic>Mites</topic><topic>Molecular evolution</topic><topic>Mortality</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Pollination</topic><topic>Positive selection</topic><topic>Prevention</topic><topic>Proteins</topic><topic>Risk factors</topic><topic>Sucrose</topic><topic>Survival</topic><topic>Varroa destructor</topic><topic>Varroidae - physiology</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Wenhao</creatorcontrib><creatorcontrib>Sun, Cheng</creatorcontrib><creatorcontrib>Lang, Haoyu</creatorcontrib><creatorcontrib>Wang, Jieni</creatorcontrib><creatorcontrib>Li, Xinyu</creatorcontrib><creatorcontrib>Guo, Jun</creatorcontrib><creatorcontrib>Zhang, Zijing</creatorcontrib><creatorcontrib>Zheng, Hao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Wenhao</au><au>Sun, Cheng</au><au>Lang, Haoyu</au><au>Wang, Jieni</au><au>Li, Xinyu</au><au>Guo, Jun</au><au>Zhang, Zijing</au><au>Zheng, Hao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Toll receptor ligand Spätzle 4 responses to the highly pathogenic Enterococcus faecalis from Varroa mites in honeybees</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2023-12-01</date><risdate>2023</risdate><volume>19</volume><issue>12</issue><spage>e1011897</spage><epage>e1011897</epage><pages>e1011897-e1011897</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Honeybees play a major role in crop pollination, which supports the agricultural economy and international food supply. The colony health of honeybees is threatened by the parasitic mite Varroa destructor, which inflicts physical injury on the hosts and serves as the vector for variable viruses. Recently, it shows that V. destructor may also transmit bacteria through the feeding wound, yet it remains unclear whether the invading bacteria can exhibit pathogenicity to the honeybees. Here, we incidentally isolate Enterococcus faecalis, one of the most abundant bacteria in Varroa mites, from dead bees during our routine generation of microbiota-free bees in the lab. In vivo tests show that E. faecalis is only pathogenic in Apis mellifera but not in Apis cerana. The expression of antimicrobial peptide genes is elevated following infection in A. cerana. The gene-based molecular evolution analysis identifies positive selection of genes encoding Späetzle 4 (Spz4) in A. cerana, a signaling protein in the Toll pathway. The amino acid sites under positive selection are related to structural changes in Spz4 protein, suggesting improvement of immunity in A. cerana. The knock-down of Spz4 in A. cerana significantly reduces the survival rates under E. faecalis challenge and the expression of antimicrobial peptide genes. Our results indicate that bacteria associated with Varroa mites are pathogenic to adult bees, and the positively selected gene Spz4 in A. cerana is crucial in response to this mite-related pathogen.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38150483</pmid><doi>10.1371/journal.ppat.1011897</doi><tpages>e1011897</tpages><orcidid>https://orcid.org/0000-0002-6446-5486</orcidid><orcidid>https://orcid.org/0000-0003-3313-1675</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino acids Analysis Animals Antimicrobial Peptides Apis mellifera Bacteria Bees Biology and Life Sciences Casualties Composition Control Diseases Enterococcal infections Enterococcus faecalis Enterococcus faecalis - genetics Evolutionary genetics Food Food supply Gene expression Genes Genetic aspects Genetic vectors Genomes Growth Health aspects Honeybee In vivo methods and tests Infections Ligands Medicine and Health Sciences Microbiota Microbiota (Symbiotic organisms) Mites Molecular evolution Mortality Pathogenicity Pathogens Pollination Positive selection Prevention Proteins Risk factors Sucrose Survival Varroa destructor Varroidae - physiology Virulence |
title | Toll receptor ligand Spätzle 4 responses to the highly pathogenic Enterococcus faecalis from Varroa mites in honeybees |
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