Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture
Abstract
Social animals are among the most successful organisms on the planet and derive many benefits from living in groups, including facilitating the evolution of agriculture. However, living in groups increases the risk of disease transmission in social animals themselves and the cultivated crops upon which they obligately depend. Social insects offer an interesting model to compare to human societies, in terms of how insects manage disease within their societies and with their agricultural symbionts. As living in large groups can help the spread of beneficial microbes as well as pathogens, we examine the role of defensive microbial symbionts in protecting the host from pathogens. We further explore how beneficial microbes may influence other pathogen defenses including behavioral and immune responses, and how we can use insect systems as models to inform on issues relating to human health and agriculture.
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1598377
- Alternate Identifier(s):
- OSTI ID: 1803405
- Grant/Contract Number:
- SC0018409
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Name: Frontiers in Microbiology Journal Volume: 11; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology; defensive symbiosis; social insects and humans; gut microbiome; colonization resistance; model systems; social immunity; insect agriculture
Citation Formats
Bratburd, Jennifer R., Arango, Rachel A., and Horn, Heidi A. Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture. Switzerland: N. p., 2020.
Web. doi:10.3389/fmicb.2020.00076.
Bratburd, Jennifer R., Arango, Rachel A., & Horn, Heidi A. Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture. Switzerland. https://doi.org/10.3389/fmicb.2020.00076
Bratburd, Jennifer R., Arango, Rachel A., and Horn, Heidi A. Fri .
"Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture". Switzerland. https://doi.org/10.3389/fmicb.2020.00076.
@article{osti_1598377,
title = {Defensive Symbioses in Social Insects Can Inform Human Health and Agriculture},
author = {Bratburd, Jennifer R. and Arango, Rachel A. and Horn, Heidi A.},
abstractNote = {Social animals are among the most successful organisms on the planet and derive many benefits from living in groups, including facilitating the evolution of agriculture. However, living in groups increases the risk of disease transmission in social animals themselves and the cultivated crops upon which they obligately depend. Social insects offer an interesting model to compare to human societies, in terms of how insects manage disease within their societies and with their agricultural symbionts. As living in large groups can help the spread of beneficial microbes as well as pathogens, we examine the role of defensive microbial symbionts in protecting the host from pathogens. We further explore how beneficial microbes may influence other pathogen defenses including behavioral and immune responses, and how we can use insect systems as models to inform on issues relating to human health and agriculture.},
doi = {10.3389/fmicb.2020.00076},
journal = {Frontiers in Microbiology},
number = ,
volume = 11,
place = {Switzerland},
year = {Fri Feb 07 00:00:00 EST 2020},
month = {Fri Feb 07 00:00:00 EST 2020}
}
https://doi.org/10.3389/fmicb.2020.00076
Web of Science
Works referenced in this record:
Gut microbial compositions mirror caste‐specific diets in a major lineage of social insects
journal, January 2019
- Otani, Saria; Zhukova, Mariya; Koné, N'golo Abdoulaye
- Environmental Microbiology Reports, Vol. 11, Issue 2
Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent Clostridium difficile infection
journal, September 2016
- Youngster, Ilan; Mahabamunuge, Jasmin; Systrom, Hannah K.
- BMC Medicine, Vol. 14, Issue 1
Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants
journal, March 2009
- Fernández-Marín, Hermógenes; Zimmerman, Jess K.; Nash, David R.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1665
The fungus-growing termite Macrotermes natalensis harbors bacillaene-producing Bacillus sp. that inhibit potentially antagonistic fungi
journal, November 2013
- Um, Soohyun; Fraimout, Antoine; Sapountzis, Panagiotis
- Scientific Reports, Vol. 3, Issue 1
Social Immunity
journal, August 2007
- Cremer, Sylvia; Armitage, Sophie A. O.; Schmid-Hempel, Paul
- Current Biology, Vol. 17, Issue 16
Close social relationships correlate with human gut microbiota composition
journal, January 2019
- Dill-McFarland, Kimberly A.; Tang, Zheng-Zheng; Kemis, Julia H.
- Scientific Reports, Vol. 9, Issue 1
Interaction between Workers during a Short Time Window Is Required for Bacterial Symbiont Transmission in Acromyrmex Leaf-Cutting Ants
journal, July 2014
- Marsh, Sarah E.; Poulsen, Michael; Pinto-Tomás, Adrián
- PLoS ONE, Vol. 9, Issue 7
Fungus-growing ants use antibiotic-producing bacteria to control garden parasites
journal, April 1999
- Currie, Cameron R.; Scott, James A.; Summerbell, Richard C.
- Nature, Vol. 398, Issue 6729
NEOLITHIC AGRICULTURE:The Slow Birth of Agriculture
journal, November 1998
- Pringle, H.
- Science, Vol. 282, Issue 5393
Homeostatic Immunity and the Microbiota
journal, April 2017
- Belkaid, Yasmine; Harrison, Oliver J.
- Immunity, Vol. 46, Issue 4
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
Architectural design influences the diversity and structure of the built environment microbiome
journal, January 2012
- Kembel, Steven W.; Jones, Evan; Kline, Jeff
- The ISME Journal, Vol. 6, Issue 8
The evolutionary and coevolutionary consequences of defensive microbes for host-parasite interactions
journal, August 2017
- King, Kayla C.; Bonsall, Michael B.
- BMC Evolutionary Biology, Vol. 17, Issue 1
Members of the human gut microbiota involved in recovery from Vibrio cholerae infection
journal, September 2014
- Hsiao, Ansel; Ahmed, A. M. Shamsir; Subramanian, Sathish
- Nature, Vol. 515, Issue 7527
Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus
journal, January 2001
- Matsuura, Kenji
- Oikos, Vol. 92, Issue 1
High Gut Microbiota Diversity Provides Lower Resistance against Infection by an Intestinal Parasite in Bumblebees
journal, August 2018
- Näpflin, Kathrin; Schmid-Hempel, Paul
- The American Naturalist, Vol. 192, Issue 2
Causes of Ecological Success: The Case of the Ants
journal, February 1987
- Wilson, Edward O.
- The Journal of Animal Ecology, Vol. 56, Issue 1
Transitional Complexity of Social Insect Immunity
journal, June 2016
- Otani, Saria; Bos, Nick; Yek, Sze H.
- Frontiers in Ecology and Evolution, Vol. 4
Weevil pgrp-lb prevents endosymbiont TCT dissemination and chronic host systemic immune activation
journal, February 2019
- Maire, Justin; Vincent-Monégat, Carole; Balmand, Séverine
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 12
Selvamicin, an atypical antifungal polyene from two alternative genomic contexts
journal, November 2016
- Van Arnam, Ethan B.; Ruzzini, Antonio C.; Sit, Clarissa S.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 46
The Evolution of Agriculture in Insects
journal, December 2005
- Mueller, Ulrich G.; Gerardo, Nicole M.; Aanen, Duur K.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 36, Issue 1
Effect of Streptomycin on Susceptibility of Intestinal Tract to Experimental Salmonella Infection.
journal, May 1954
- Bohnhoff, M.; Drake, B. L.; Miller, C. P.
- Experimental Biology and Medicine, Vol. 86, Issue 1
The Tsetse Fly Displays an Attenuated Immune Response to Its Secondary Symbiont, Sodalis glossinidius
journal, July 2019
- Trappeniers, Katrien; Matetovici, Irina; Van Den Abbeele, Jan
- Frontiers in Microbiology, Vol. 10
Simply put: Vaccination saves lives
journal, April 2017
- Orenstein, Walter A.; Ahmed, Rafi
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 16
Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses
journal, November 2012
- Nyholm, Spencer V.; Graf, Joerg
- Nature Reviews Microbiology, Vol. 10, Issue 12
The Ambrosia Symbiosis: From Evolutionary Ecology to Practical Management
journal, January 2017
- Hulcr, Jiri; Stelinski, Lukasz L.
- Annual Review of Entomology, Vol. 62, Issue 1
Microbiota and the social brain
journal, October 2019
- Sherwin, Eoin; Bordenstein, Seth R.; Quinn, John L.
- Science, Vol. 366, Issue 6465
A Systematic Analysis of Biosynthetic Gene Clusters in the Human Microbiome Reveals a Common Family of Antibiotics
journal, September 2014
- Donia, Mohamed S.; Cimermancic, Peter; Schulze, Christopher J.
- Cell, Vol. 158, Issue 6
The agricultural pathology of ant fungus gardens
journal, July 1999
- Currie, C. R.; Mueller, U. G.; Malloch, D.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 14
Functional diversity within the simple gut microbiota of the honey bee
journal, June 2012
- Engel, P.; Martinson, V. G.; Moran, N. A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
The Microbiome and Host Behavior
journal, July 2017
- Vuong, Helen E.; Yano, Jessica M.; Fung, Thomas C.
- Annual Review of Neuroscience, Vol. 40, Issue 1
Socially transmitted gut microbiota protect bumble bees against an intestinal parasite
journal, November 2011
- Koch, H.; Schmid-Hempel, P.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 48
Transmission modes of the mammalian gut microbiota
journal, October 2018
- Moeller, Andrew H.; Suzuki, Taichi A.; Phifer-Rixey, Megan
- Science, Vol. 362, Issue 6413
Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis
journal, March 2009
- Oh, Dong-Chan; Poulsen, Michael; Currie, Cameron R.
- Nature Chemical Biology, Vol. 5, Issue 6
Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers
journal, August 2016
- Schwarz, Ryan S.; Moran, Nancy A.; Evans, Jay D.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 33
Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus)
journal, April 2014
- Cariveau, Daniel P.; Elijah Powell, J.; Koch, Hauke
- The ISME Journal, Vol. 8, Issue 12
The Effect of Density-Dependent Phase on the Locust Gut Bacterial Composition
journal, January 2019
- Lavy, Omer; Gophna, Uri; Gefen, Eran
- Frontiers in Microbiology, Vol. 9
Antivirulence Activity of the Human Gut Metabolome
journal, July 2014
- Antunes, L. Caetano M.; McDonald, Julie A. K.; Schroeter, Kathleen
- mBio, Vol. 5, Issue 4
Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria
journal, November 2010
- Cafaro, Matías J.; Poulsen, Michael; Little, Ainslie E. F.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1713
Treating Clostridium difficile Infection With Fecal Microbiota Transplantation
journal, December 2011
- Bakken, Johan S.; Borody, Thomas; Brandt, Lawrence J.
- Clinical Gastroenterology and Hepatology, Vol. 9, Issue 12
The evolution of uniparental transmission of fungal symbionts in fungus-growing termites (Macrotermitinae)
journal, January 2003
- Korb, Judith; Aanen, Duur K.
- Behavioral Ecology and Sociobiology, Vol. 53, Issue 2
Benefaction of probiotics for human health: A review
journal, July 2018
- George Kerry, Rout; Patra, Jayanta Kumar; Gouda, Sushanto
- Journal of Food and Drug Analysis, Vol. 26, Issue 3
A neuropterous larva uses an allomone to attack termites
journal, February 1981
- Johnson, J. B.; Hagen, K. S.
- Nature, Vol. 289, Issue 5797
The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates
journal, October 2016
- Khadempour, Lily; Burnum-Johnson, Kristin E.; Baker, Erin S.
- Molecular Ecology, Vol. 25, Issue 22
The antimicrobial potential of Streptomyces from insect microbiomes
journal, January 2019
- Chevrette, Marc G.; Carlson, Caitlin M.; Ortega, Humberto E.
- Nature Communications, Vol. 10, Issue 1
Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites
journal, April 2003
- Currie, C. R.; Bot, A. N. M.; Boomsma, J. J.
- Oikos, Vol. 101, Issue 1
US Immigration Westernizes the Human Gut Microbiome
journal, November 2018
- Vangay, Pajau; Johnson, Abigail J.; Ward, Tonya L.
- Cell, Vol. 175, Issue 4
Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees
journal, March 2017
- Raymann, Kasie; Shaffer, Zack; Moran, Nancy A.
- PLOS Biology, Vol. 15, Issue 3
Vulnerability of the industrialized microbiota
journal, October 2019
- Sonnenburg, Justin L.; Sonnenburg, Erica D.
- Science, Vol. 366, Issue 6464
Dirt, disgust and disease: a natural history of hygiene
journal, August 2007
- Curtis, V. A.
- Journal of Epidemiology & Community Health, Vol. 61, Issue 8
Long-term ecological impacts of antibiotic administration on the human intestinal microbiota
journal, May 2007
- Jernberg, Cecilia; Löfmark, Sonja; Edlund, Charlotta
- The ISME Journal, Vol. 1, Issue 1
Understanding the mechanisms of faecal microbiota transplantation
journal, June 2016
- Khoruts, Alexander; Sadowsky, Michael J.
- Nature Reviews Gastroenterology & Hepatology, Vol. 13, Issue 9
Antibiotic and Antimalarial Quinones from Fungus-Growing Ant-Associated Pseudonocardia sp.
journal, October 2012
- Carr, Gavin; Derbyshire, Emily R.; Caldera, Eric
- Journal of Natural Products, Vol. 75, Issue 10
Antibiotics, birth mode, and diet shape microbiome maturation during early life
journal, June 2016
- Bokulich, Nicholas A.; Chung, Jennifer; Battaglia, Thomas
- Science Translational Medicine, Vol. 8, Issue 343
Genome Sequence of the Pea Aphid Acyrthosiphon pisum
journal, February 2010
- ,
- PLoS Biology, Vol. 8, Issue 2
How the insect immune system interacts with an obligate symbiotic bacterium
journal, August 2010
- Douglas, A. E.; Bouvaine, S.; Russell, R. R.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1704
Social immunity and the evolution of group living in insects
journal, May 2015
- Meunier, Joël
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 370, Issue 1669
Evolutionary feedbacks between insect sociality and microbial management
journal, August 2017
- Biedermann, Peter HW; Rohlfs, Marko
- Current Opinion in Insect Science, Vol. 22
The core gut microbiome, energy balance and obesity: The core gut microbiome, energy balance and obesity
journal, August 2009
- Turnbaugh, Peter J.; Gordon, Jeffrey I.
- The Journal of Physiology, Vol. 587, Issue 17
Kin recognition in Drosophila: the importance of ecology and gut microbiota
journal, September 2013
- Lizé, Anne; McKay, Raegan; Lewis, Zenobia
- The ISME Journal, Vol. 8, Issue 2
Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms
journal, January 2015
- Flórez, Laura V.; Biedermann, Peter H. W.; Engl, Tobias
- Natural Product Reports, Vol. 32, Issue 7
Role of Microorganisms in the Digestion of Lignocellulose by Termites
journal, January 1994
- Breznak, J. A.; Brune, A.
- Annual Review of Entomology, Vol. 39, Issue 1
Evolutionary stability of antibiotic protection in a defensive symbiosis
journal, February 2018
- Engl, Tobias; Kroiss, Johannes; Kai, Marco
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 9
Are societies resilient? Challenges faced by social insects in a changing world
journal, October 2018
- Fisher, Kaleigh; West, Mari; Lomeli, Adriana M.
- Insectes Sociaux, Vol. 66, Issue 1
Convergent evolution of complex structures for ant–bacterial defensive symbiosis in fungus-farming ants
journal, October 2018
- Li, Hongjie; Sosa-Calvo, Jeffrey; Horn, Heidi A.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 42
Human commensals producing a novel antibiotic impair pathogen colonization
journal, July 2016
- Zipperer, Alexander; Konnerth, Martin C.; Laux, Claudia
- Nature, Vol. 535, Issue 7613
Human Population: The Next Half Century
journal, November 2003
- Cohen, J. E.
- Science, Vol. 302, Issue 5648
Grooming Behavior as a Mechanism of Insect Disease Defense
journal, November 2013
- Zhukovskaya, Marianna; Yanagawa, Aya; Forschler, Brian
- Insects, Vol. 4, Issue 4
Human Gut Microbiota Predicts Susceptibility to Vibrio cholerae Infection
journal, April 2018
- Midani, Firas S.; Weil, Ana A.; Chowdhury, Fahima
- The Journal of Infectious Diseases, Vol. 218, Issue 4
Cellulase genes from the parabasalian symbiont Pseudotrichonympha grassii in the hindgut of the wood-feeding termite Coptotermes formosanus
journal, October 2002
- Nakashima, K.; Watanabe, H.; Azuma, J. -I.
- Cellular and Molecular Life Sciences (CMLS), Vol. 59, Issue 9
Major evolutionary transitions in ant agriculture
journal, March 2008
- Schultz, T. R.; Brady, S. G.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 14
Population biology of infectious diseases: Part I
journal, August 1979
- Anderson, Roy M.; May, Robert M.
- Nature, Vol. 280, Issue 5721
Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants: Parasite-defence interactions in leaf-cutting ants
journal, November 2009
- Poulsen, Michael; Cafaro, Matías J.; Erhardt, Daniel P.
- Environmental Microbiology Reports, Vol. 2, Issue 4
Colony size evolution in ants: macroevolutionary trends
journal, February 2016
- Burchill, A. T.; Moreau, C. S.
- Insectes Sociaux, Vol. 63, Issue 2
Transmission of human-associated microbiota along family and social networks
journal, March 2019
- Brito, Ilana L.; Gurry, Thomas; Zhao, Shijie
- Nature Microbiology, Vol. 4, Issue 6
Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies
journal, November 2003
- Altizer, Sonia; Nunn, Charles L.; Thrall, Peter H.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 34, Issue 1
A Brief History of the Antibiotic Era: Lessons Learned and Challenges for the Future
journal, January 2010
- Aminov, Rustam I.
- Frontiers in Microbiology, Vol. 1
Chemical and genetic defenses against disease in insect societies
journal, October 2008
- Stow, Adam; Beattie, Andrew
- Brain, Behavior, and Immunity, Vol. 22, Issue 7
Why does the microbiome affect behaviour?
journal, April 2018
- Johnson, Katerina V. -A.; Foster, Kevin R.
- Nature Reviews Microbiology, Vol. 16, Issue 10
Bacterial symbionts in agricultural systems provide a strategic source for antibiotic discovery
journal, August 2013
- Ramadhar, Timothy R.; Beemelmanns, Christine; Currie, Cameron R.
- The Journal of Antibiotics, Vol. 67, Issue 1