Skip to main content

Main menu

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
  • Submit
  • About
    • Editorial Board
    • PNAS Staff
    • FAQ
    • Accessibility Statement
    • Rights and Permissions
    • Site Map
  • Contact
  • Journal Club
  • Subscribe
    • Subscription Rates
    • Subscriptions FAQ
    • Open Access
    • Recommend PNAS to Your Librarian

User menu

  • Log in
  • My Cart

Search

  • Advanced search
Home
Home
  • Log in
  • My Cart

Advanced Search

  • Home
  • Articles
    • Current
    • Special Feature Articles - Most Recent
    • Special Features
    • Colloquia
    • Collected Articles
    • PNAS Classics
    • List of Issues
  • Front Matter
    • Front Matter Portal
    • Journal Club
  • News
    • For the Press
    • This Week In PNAS
    • PNAS in the News
  • Podcasts
  • Authors
    • Information for Authors
    • Editorial and Journal Policies
    • Submission Procedures
    • Fees and Licenses
  • Submit
Perspective

Animals in a bacterial world, a new imperative for the life sciences

Margaret McFall-Ngai, Michael G. Hadfield, Thomas C. G. Bosch, Hannah V. Carey, Tomislav Domazet-Lošo, Angela E. Douglas, Nicole Dubilier, Gerard Eberl, Tadashi Fukami, Scott F. Gilbert, Ute Hentschel, Nicole King, Staffan Kjelleberg, Andrew H. Knoll, Natacha Kremer, Sarkis K. Mazmanian, Jessica L. Metcalf, Kenneth Nealson, Naomi E. Pierce, John F. Rawls, Ann Reid, Edward G. Ruby, Mary Rumpho, Jon G. Sanders, Diethard Tautz, and Jennifer J. Wernegreen
  1. aDepartment of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706;
  2. bKewalo Marine Laboratory, University of Hawaii, Honolulu, HI 96813;
  3. cZoological Institute, Christian-Albrechts-University, D-24098 Kiel, Germany;
  4. dDepartment of Comparative Biosciences, University of Wisconsin, Madison, WI 53706;
  5. eRuđer Bošković Institute, HR-10000 Zagreb, Croatia;
  6. fDepartment of Entomology and Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853;
  7. gMax Planck Institute for Marine Microbiology, Symbiosis Group, D-28359 Bremen, Germany;
  8. hLymphoid Tissue Development Unit, Institut Pasteur, 75724 Paris, France;
  9. iDepartment of Biology, Stanford University, Stanford, CA 94305;
  10. jBiotechnology Institute, University of Helsinki, Helsinki 00014, Finland;
  11. kJulius-von-Sachs Institute, University of Wuerzburg, D-97082 Wuezburg, Germany;
  12. lMolecular and Cell Biology, University of California, Berkeley, CA 94720;
  13. mSingapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University, Singapore 637551, and Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney 2052, Australia;
  14. nBotanical Museum, Harvard University, Cambridge, MA 02138;
  15. oDivision of Biology, California Institute of Technology, Pasadena CA 91125;
  16. pBiofrontiers Institute, University of Colorado, Boulder CO 80309;
  17. qDepartment of Earth Sciences, University of Southern California, Los Angeles, CA 90089;
  18. rDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
  19. sCell Biology and Physiology, University of North Carolina, Chapel Hill, NC 27599;
  20. tAmerican Academy of Microbiology, Washington, DC 20036;
  21. uDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269;
  22. vDepartment of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, D-24306 Plön, Germany; and
  23. wNicholas School and Institute for Genome Sciences and Policy, Duke University, Durham, NC 27708

See allHide authors and affiliations

PNAS first published February 7, 2013; https://doi.org/10.1073/pnas.1218525110
Margaret McFall-Ngai
aDepartment of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: mjmcfallngai@wisc.edu hadfield@hawaii.edu
Michael G. Hadfield
bKewalo Marine Laboratory, University of Hawaii, Honolulu, HI 96813;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: mjmcfallngai@wisc.edu hadfield@hawaii.edu
Thomas C. G. Bosch
cZoological Institute, Christian-Albrechts-University, D-24098 Kiel, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hannah V. Carey
dDepartment of Comparative Biosciences, University of Wisconsin, Madison, WI 53706;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tomislav Domazet-Lošo
eRuđer Bošković Institute, HR-10000 Zagreb, Croatia;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Angela E. Douglas
fDepartment of Entomology and Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nicole Dubilier
gMax Planck Institute for Marine Microbiology, Symbiosis Group, D-28359 Bremen, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Gerard Eberl
hLymphoid Tissue Development Unit, Institut Pasteur, 75724 Paris, France;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Tadashi Fukami
iDepartment of Biology, Stanford University, Stanford, CA 94305;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Scott F. Gilbert
jBiotechnology Institute, University of Helsinki, Helsinki 00014, Finland;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ute Hentschel
kJulius-von-Sachs Institute, University of Wuerzburg, D-97082 Wuezburg, Germany;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Nicole King
lMolecular and Cell Biology, University of California, Berkeley, CA 94720;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Staffan Kjelleberg
mSingapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University, Singapore 637551, and Centre for Marine Bio-Innovation and School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney 2052, Australia;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Andrew H. Knoll
nBotanical Museum, Harvard University, Cambridge, MA 02138;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Natacha Kremer
aDepartment of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sarkis K. Mazmanian
oDivision of Biology, California Institute of Technology, Pasadena CA 91125;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jessica L. Metcalf
pBiofrontiers Institute, University of Colorado, Boulder CO 80309;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kenneth Nealson
qDepartment of Earth Sciences, University of Southern California, Los Angeles, CA 90089;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Naomi E. Pierce
rDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
John F. Rawls
sCell Biology and Physiology, University of North Carolina, Chapel Hill, NC 27599;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ann Reid
tAmerican Academy of Microbiology, Washington, DC 20036;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Edward G. Ruby
aDepartment of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Mary Rumpho
uDepartment of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jon G. Sanders
rDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Diethard Tautz
vDepartment of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, D-24306 Plön, Germany; and
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jennifer J. Wernegreen
wNicholas School and Institute for Genome Sciences and Policy, Duke University, Durham, NC 27708
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved January 17, 2013 (received for review December 2, 2012)

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF
Loading

Abstract

In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

  • bacterial roles animal origins
  • reciprocal effects animal–bacterial genomics
  • bacteria-driven development
  • microbiome and host physiology
  • nested ecosystems

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: mjmcfallngai{at}wisc.edu or hadfield{at}hawaii.edu.
  • Author contributions: M.M.-N., M.G.H., T.C.G.B., H.V.C., T.D.-L., A.E.D., N.D., G.E., T.F., S.F.G., U.H., N. King, S.K., A.H.K., N. Kremer, S.K.M., J.L.M., K.N., N.E.P., J.F.R., A.R., E.G.R., M.R., J.G.S., D.T., and J.J.W. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1218525110/-/DCSupplemental.

Next
Back to top
Article Alerts
Email Article

Thank you for your interest in spreading the word on PNAS.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Animals in a bacterial world, a new imperative for the life sciences
(Your Name) has sent you a message from PNAS
(Your Name) thought you would like to see the PNAS web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Citation Tools
Animals in a bacterial world
Margaret McFall-Ngai, Michael G. Hadfield, Thomas C. G. Bosch, Hannah V. Carey, Tomislav Domazet-Lošo, Angela E. Douglas, Nicole Dubilier, Gerard Eberl, Tadashi Fukami, Scott F. Gilbert, Ute Hentschel, Nicole King, Staffan Kjelleberg, Andrew H. Knoll, Natacha Kremer, Sarkis K. Mazmanian, Jessica L. Metcalf, Kenneth Nealson, Naomi E. Pierce, John F. Rawls, Ann Reid, Edward G. Ruby, Mary Rumpho, Jon G. Sanders, Diethard Tautz, Jennifer J. Wernegreen
Proceedings of the National Academy of Sciences Feb 2013, 201218525; DOI: 10.1073/pnas.1218525110

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Request Permissions
Share
Animals in a bacterial world
Margaret McFall-Ngai, Michael G. Hadfield, Thomas C. G. Bosch, Hannah V. Carey, Tomislav Domazet-Lošo, Angela E. Douglas, Nicole Dubilier, Gerard Eberl, Tadashi Fukami, Scott F. Gilbert, Ute Hentschel, Nicole King, Staffan Kjelleberg, Andrew H. Knoll, Natacha Kremer, Sarkis K. Mazmanian, Jessica L. Metcalf, Kenneth Nealson, Naomi E. Pierce, John F. Rawls, Ann Reid, Edward G. Ruby, Mary Rumpho, Jon G. Sanders, Diethard Tautz, Jennifer J. Wernegreen
Proceedings of the National Academy of Sciences Feb 2013, 201218525; DOI: 10.1073/pnas.1218525110
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Mendeley logo Mendeley
Proceedings of the National Academy of Sciences: 118 (9)
Current Issue

Submit

Sign up for Article Alerts

Jump to section

  • Article
  • Figures & SI
  • Info & Metrics
  • PDF

You May Also be Interested in

Setting sun over a sun-baked dirt landscape
Core Concept: Popular integrated assessment climate policy models have key caveats
Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Model of the Amazon forest
News Feature: A sea in the Amazon
Did the Caribbean sweep into the western Amazon millions of years ago, shaping the region’s rich biodiversity?
Image credit: Tacio Cordeiro Bicudo (University of São Paulo, São Paulo, Brazil), Victor Sacek (University of São Paulo, São Paulo, Brazil), and Lucy Reading-Ikkanda (artist).
Syrian archaeological site
Journal Club: In Mesopotamia, early cities may have faltered before climate-driven collapse
Settlements 4,200 years ago may have suffered from overpopulation before drought and lower temperatures ultimately made them unsustainable.
Image credit: Andrea Ricci.
Steamboat Geyser eruption.
Eruption of Steamboat Geyser
Mara Reed and Michael Manga explore why Yellowstone's Steamboat Geyser resumed erupting in 2018.
Listen
Past PodcastsSubscribe
Birds nestling on tree branches
Parent–offspring conflict in songbird fledging
Some songbird parents might improve their own fitness by manipulating their offspring into leaving the nest early, at the cost of fledgling survival, a study finds.
Image credit: Gil Eckrich (photographer).

Similar Articles

Site Logo
Powered by HighWire
  • Submit Manuscript
  • Twitter
  • Facebook
  • RSS Feeds
  • Email Alerts

Articles

  • Current Issue
  • Special Feature Articles – Most Recent
  • List of Issues

PNAS Portals

  • Anthropology
  • Chemistry
  • Classics
  • Front Matter
  • Physics
  • Sustainability Science
  • Teaching Resources

Information

  • Authors
  • Editorial Board
  • Reviewers
  • Subscribers
  • Librarians
  • Press
  • Site Map
  • PNAS Updates
  • FAQs
  • Accessibility Statement
  • Rights & Permissions
  • About
  • Contact

Feedback    Privacy/Legal

Copyright © 2021 National Academy of Sciences. Online ISSN 1091-6490