Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes.

Kevin R Theis, Nolwenn M Dheilly, Jonathan L Klassen, Robert M Brucker, John F Baines, Thomas C G Bosch, John F Cryan, Scott F Gilbert, Charles J Goodnight, Elisabeth A Lloyd, Jan Sapp, Philippe Vandenkoornhuyse, Ilana Zilber-Rosenberg, Eugene Rosenberg, Seth R Bordenstein
Author Information
  1. Kevin R Theis: Department of Immunology and Microbiology, Wayne State University, Detroit, Michigan, USA; Wayne State University Perinatal Initiative, Detroit, Michigan, USA. ORCID
  2. Nolwenn M Dheilly: School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, New York, USA. ORCID
  3. Jonathan L Klassen: Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA. ORCID
  4. Robert M Brucker: The Rowland Institute at Harvard, Harvard University, Cambridge, Massachusetts, USA. ORCID
  5. John F Baines: Max Planck Institute for Evolutionary Biology, Plön, Germany; Institute for Experimental Medicine, Christian Albrechts University of Kiel, Kiel, Germany. ORCID
  6. Thomas C G Bosch: Zoological Institute, Christian Albrechts University, Kiel, Germany.
  7. John F Cryan: Department of Anatomy and Neuroscience, University College Cork, Cork, Ireland; APC Microbiome Institute, University College Cork, Cork, Ireland. ORCID
  8. Scott F Gilbert: Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, USA.
  9. Charles J Goodnight: Department of Biology, University of Vermont, Burlington, Vermont, USA. ORCID
  10. Elisabeth A Lloyd: History and Philosophy of Science Department, Indiana University, Bloomington, Indiana, USA. ORCID
  11. Jan Sapp: Department of Biology, York University, Toronto, Ontario, Canada.
  12. Philippe Vandenkoornhuyse: Université de Rennes 1, CNRS, UMR6553 EcoBio, Rennes, France. ORCID
  13. Ilana Zilber-Rosenberg: Independent Researcher, Givat Shmuel, Israel.
  14. Eugene Rosenberg: Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Tel Aviv, Israel.
  15. Seth R Bordenstein: Departments of Biological Sciences and Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA. ORCID

Abstract

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization-what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.

Keywords

References

  1. Evolution. 2006 May;60(5):991-1003 [PMID: 16817539]
  2. Symbiosis. 1991;11:93-101 [PMID: 11538111]
  3. Biosystems. 1992;27(1):53-62 [PMID: 1391691]
  4. Trends Microbiol. 2015 Oct;23(10):606-17 [PMID: 26422463]
  5. Science. 2015 Sep 11;349(6253):1172-3 [PMID: 26359393]
  6. ISME J. 2016 May;10 (5):1157-69 [PMID: 26555246]
  7. PLoS Biol. 2015 Aug 18;13(8):e1002226 [PMID: 26284777]
  8. Ecol Lett. 2006 Jan;9(1):78-85 [PMID: 16958871]
  9. Infect Immun. 2015 Jan;83(1):2-7 [PMID: 25385796]
  10. Zoology (Jena). 2011 Sep;114(4):185-90 [PMID: 21737250]
  11. Birth Defects Res C Embryo Today. 2011 Mar;93(1):56-66 [PMID: 21425442]
  12. Environ Microbiol. 2009 Dec;11(12):2959-62 [PMID: 19573132]
  13. New Phytol. 2013 Apr;198(2):347-85 [PMID: 23437795]
  14. Nat Rev Genet. 2006 Jul;7(7):510-23 [PMID: 16778835]
  15. Front Microbiol. 2015 Aug 04;6:697 [PMID: 26300848]
  16. New Phytol. 2015 Jun;206(4):1196-206 [PMID: 25655016]
  17. Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13146-51 [PMID: 17664430]
  18. PLoS Biol. 2015 Dec 04;13(12):e1002311 [PMID: 26636661]
  19. Evolution. 2012 Feb;66(2):349-62 [PMID: 22276533]
  20. Trends Ecol Evol. 2012 Aug;27(8):443-51 [PMID: 22541872]
  21. Infect Genet Evol. 2015 Aug;34:251-9 [PMID: 26026593]
  22. Proc Natl Acad Sci U S A. 2013 Sep 24;110(39):E3730-8 [PMID: 24003149]
  23. Science. 2013 Aug 9;341(6146):667-9 [PMID: 23868918]
  24. Proc Natl Acad Sci U S A. 2013 Feb 26;110(9):3229-36 [PMID: 23391737]
  25. FEMS Microbiol Rev. 2008 Aug;32(5):723-35 [PMID: 18549407]
  26. Philos Trans R Soc Lond B Biol Sci. 2011 May 12;366(1569):1401-9 [PMID: 21444314]
  27. Science. 2014 Aug 29;345(6200):1011 [PMID: 25170144]
  28. Environ Microbiol Rep. 2010 Aug;2(4):500-6 [PMID: 23766221]
  29. Front Microbiol. 2014 Feb 24;5:46 [PMID: 24605109]

Word Cloud

Created with Highcharts 10.0.0hologenomelevelsvocabularydiscoursecritiquingconceptselectionmicrobiomeGivencomplexityhost-microbiotasymbiosesscientistsphilosophersaskingquestionsnewbiologicalhierarchicalorganization-whatholobionthologenome?applied?conceptsnullhypothesishost-microbesystemslimitedcertainspectrumsymbioticinteractionshost-microbialcoevolution?CriticalnecessarynascentareaproductiverequiresskepticsproponentsuselexiconinstancesynonymouscoevolutionarguingentityprimaryunitdismissesfactalwaysembracedmultilevelHolobiontshologenomesincontrovertiblemultipartiteentitiesresultecologicalevolutionarygeneticprocessesvariousrestrictedonespecialprocessconstitutewiderframeworkhostbiologylightGettingHologenomeConceptRight:Eco-EvolutionaryFrameworkHostsMicrobiomesecologyevolution

Similar Articles

Cited By (197)