Tailed bacteriophages (Caudoviricetes) dominate the microbiome of a diseased stingless bee.

Lilian Caesar, Karen Luisa Haag
Author Information
  1. Lilian Caesar: Indiana University Bloomington, Department of Biology, Bloomington, IN, USA. ORCID
  2. Karen Luisa Haag: Universidade Federal do Rio Grande do Sul, Departamento de Gen��tica, Programa de P��s-Gradua����o em Gen��tica e Biologia Molecular, Porto Alegre, RS, Brazil. ORCID

Abstract

Bacteriophages, viruses that infect bacterial hosts, are known to rule the dynamics and diversity of bacterial populations in a number of ecosystems. Bacterial communities residing in the gut of animals, known as the gut microbiome, have revolutionized our understanding of many diseases. However, the gut phageome, while of apparent importance in this context, remains an underexplored area of research. Here we identify for the first time genomic sequences from tailed viruses (Caudoviricetes) that are associated with the microbiome of stingless bees (Melipona quadrifasciata). Both DNA and RNA were extracted from virus particles isolated from healthy and diseased forager bees, the latter showing symptoms from an annual syndrome that only affects M. quadrifasciata. Viral contigs from previously sequenced metagenomes of healthy and diseased forager bees were used for the analyses. Using conserved proteins deduced from their genomes, we found that Caudoviricetes were only present in the worker bee gut microbiome from diseased stingless bees. The most abundant phages are phylogenetically related to phages that infect Gram-positive bacteria from the order Lactobacillales and Gram-negative bacteria from the genus Gilliamella and Bartonella, that are common honey bee symbionts. The potential implication of these viruses in the M. quadrifasciata syndrome is discussed.

References

  1. Curr Opin Virol. 2019 Aug;37:63-71 [PMID: 31295677]
  2. Nat Biotechnol. 2019 Jan;37(1):29-37 [PMID: 30556814]
  3. Nat Biotechnol. 2021 May;39(5):578-585 [PMID: 33349699]
  4. Front Cell Infect Microbiol. 2021 Jun 04;11:643214 [PMID: 34150671]
  5. mBio. 2023 Apr 25;14(2):e0353822 [PMID: 36939321]
  6. Front Microbiol. 2022 Dec 16;13:1032186 [PMID: 36590402]
  7. J Invertebr Pathol. 2017 Feb;143:35-39 [PMID: 27887862]
  8. Nature. 1999 Jun 10;399(6736):541-8 [PMID: 10376593]
  9. Microbiome. 2021 Feb 1;9(1):37 [PMID: 33522966]
  10. Microb Ecol. 2023 May;85(4):1514-1526 [PMID: 35513592]
  11. Lab Anim (NY). 2018 Nov;47(11):317-325 [PMID: 30353179]
  12. Nat Biotechnol. 2024 Aug;42(8):1303-1312 [PMID: 37735266]
  13. BMC Bioinformatics. 2010 Mar 08;11:119 [PMID: 20211023]
  14. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  15. Proc Natl Acad Sci U S A. 2020 Mar 31;117(13):7355-7362 [PMID: 32179689]
  16. Bioinformatics. 2014 Jul 15;30(14):2068-9 [PMID: 24642063]
  17. Nat Biotechnol. 2019 Jun;37(6):632-639 [PMID: 31061483]
  18. J Gen Virol. 2019 Jul;100(7):1153-1164 [PMID: 31169486]
  19. mSystems. 2022 Apr 26;7(2):e0119521 [PMID: 35343797]
  20. Nat Biotechnol. 2017 Nov;35(11):1026-1028 [PMID: 29035372]
  21. Mol Biol Evol. 2013 Apr;30(4):772-80 [PMID: 23329690]
  22. Proc Natl Acad Sci U S A. 2020 May 12;117(19):10511-10519 [PMID: 32341166]
  23. Nucleic Acids Res. 2021 Apr 6;49(6):3127-3138 [PMID: 33677572]
  24. Nat Rev Microbiol. 2022 Dec;20(12):737-749 [PMID: 35773472]
  25. ISME J. 2021 Sep;15(9):2813-2816 [PMID: 34007058]
  26. Nat Rev Microbiol. 2005 Jun;3(6):504-10 [PMID: 15886693]
  27. ISME J. 2017 Dec;11(12):2864-2868 [PMID: 28742071]
  28. Viruses. 2013 Mar 11;5(3):806-23 [PMID: 23478639]
  29. Nucleic Acids Res. 2022 Aug 12;50(14):e83 [PMID: 35544285]
  30. Syst Biol. 2003 Oct;52(5):696-704 [PMID: 14530136]
  31. Nat Methods. 2012 Mar 04;9(4):357-9 [PMID: 22388286]

Word Cloud

Created with Highcharts 10.0.0gutmicrobiomebeesdiseasedvirusesCaudoviricetesstinglessquadrifasciatabeeinfectbacterialknownhealthyforagersyndromeMphagesbacteriaBacteriophageshostsruledynamicsdiversitypopulationsnumberecosystemsBacterialcommunitiesresidinganimalsrevolutionizedunderstandingmanydiseasesHoweverphageomeapparentimportancecontextremainsunderexploredarearesearchidentifyfirsttimegenomicsequencestailedassociatedMeliponaDNARNAextractedvirusparticlesisolatedlattershowingsymptomsannualaffectsViralcontigspreviouslysequencedmetagenomesusedanalysesUsingconservedproteinsdeducedgenomesfoundpresentworkerabundantphylogeneticallyrelatedGram-positiveorderLactobacillalesGram-negativegenusGilliamellaBartonellacommonhoneysymbiontspotentialimplicationdiscussedTailedbacteriophagesdominate

Similar Articles

Cited By (2)