Microbiomes Reduce Their Host’s Sensitivity to Interspecific Interactions
Abstract
Bacteria associated with eukaryotic hosts can affect host fitness and trophic interactions between eukaryotes, but the extent to which bacteria influence the eukaryotic species interactions within trophic levels that modulate biodiversity and species coexistence is mostly unknown. Here, we used phytoplankton, which are a classic model for evaluating interactions between species, grown with and without associated bacteria to test whether the bacteria alter the strength and type of species interactions within a trophic level. We demonstrate that host-associated bacteria alter host growth rates and carrying capacity. This did not change the type but frequently changed the strength of host interspecific interactions by facilitating host growth in the presence of an established species. These findings indicate that microbiomes can regulate their host species’ interspecific interactions. As between-species interaction strength impacts their ability to coexist, our findings show that microbiomes have the potential to modulate eukaryotic species diversity and community composition.
- Authors:
-
[1];
- Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA
- School for Environment and Sustainability, University of Michigan, Ann Arbor, Michigan, USA, Cooperative Institute for Great Lakes Research, University of Michigan, Ann Arbor, Michigan, USA
- Publication Date:
- Research Org.:
- Univ. of Michigan, Ann Arbor, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1592504
- Alternate Identifier(s):
- OSTI ID: 1626151
- Grant/Contract Number:
- DOE F052906; FG02-00ER41132
- Resource Type:
- Published Article
- Journal Name:
- mBio
- Additional Journal Information:
- Journal Name: mBio Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2161-2129
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Microbiology; microbiome; eukaryotic species interactions; species coexistence; biodiversity
Citation Formats
Jackrel, Sara L., Schmidt, Kathryn C., Cardinale, Bradley J., Denef, Vincent J., and Cooper, ed., Vaughn S. Microbiomes Reduce Their Host’s Sensitivity to Interspecific Interactions. United States: N. p., 2020.
Web. doi:10.1128/mBio.02657-19.
Jackrel, Sara L., Schmidt, Kathryn C., Cardinale, Bradley J., Denef, Vincent J., & Cooper, ed., Vaughn S. Microbiomes Reduce Their Host’s Sensitivity to Interspecific Interactions. United States. https://doi.org/10.1128/mBio.02657-19
Jackrel, Sara L., Schmidt, Kathryn C., Cardinale, Bradley J., Denef, Vincent J., and Cooper, ed., Vaughn S. Tue .
"Microbiomes Reduce Their Host’s Sensitivity to Interspecific Interactions". United States. https://doi.org/10.1128/mBio.02657-19.
@article{osti_1592504,
title = {Microbiomes Reduce Their Host’s Sensitivity to Interspecific Interactions},
author = {Jackrel, Sara L. and Schmidt, Kathryn C. and Cardinale, Bradley J. and Denef, Vincent J. and Cooper, ed., Vaughn S.},
abstractNote = {Bacteria associated with eukaryotic hosts can affect host fitness and trophic interactions between eukaryotes, but the extent to which bacteria influence the eukaryotic species interactions within trophic levels that modulate biodiversity and species coexistence is mostly unknown. Here, we used phytoplankton, which are a classic model for evaluating interactions between species, grown with and without associated bacteria to test whether the bacteria alter the strength and type of species interactions within a trophic level. We demonstrate that host-associated bacteria alter host growth rates and carrying capacity. This did not change the type but frequently changed the strength of host interspecific interactions by facilitating host growth in the presence of an established species. These findings indicate that microbiomes can regulate their host species’ interspecific interactions. As between-species interaction strength impacts their ability to coexist, our findings show that microbiomes have the potential to modulate eukaryotic species diversity and community composition.},
doi = {10.1128/mBio.02657-19},
journal = {mBio},
number = 1,
volume = 11,
place = {United States},
year = {Tue Feb 25 00:00:00 EST 2020},
month = {Tue Feb 25 00:00:00 EST 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1128/mBio.02657-19
https://doi.org/10.1128/mBio.02657-19
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 15 works
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
FIG 1: (A) Micrographs depicting the presence and absence of phytoplankton-associated bacteria prior to and after using our axenification protocol on Chlorella sorokiniana. Samples were stained with DAPI (4',6-diamidino-2-phenylindole) and viewed at a x 100 magnification with an oil immersion lens on a Zeiss AxioImager M2 epifluorescence microscope. Bacteria andmore »
All figures and tables
(3 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
The influence of phylogenetic relatedness on species interactions among freshwater green algae in a mesocosm experiment
journal, June 2014
- Venail, Patrick A.; Narwani, Anita; Fritschie, Keith
- Journal of Ecology, Vol. 102, Issue 5
Soil microbial communities alter conspecific and congeneric competition consistent with patterns of field coexistence in three Trifolium congeners
journal, August 2018
- Siefert, Andrew; Zillig, Kenneth W.; Friesen, Maren L.
- Journal of Ecology, Vol. 106, Issue 5
Stimulation of Alexandrium fundyense growth by bacterial assemblages from the Bay of Fundy
journal, April 2002
- Ferrier, M.; Martin, J. L.; Rooney-Varga, J. N.
- Journal of Applied Microbiology, Vol. 92, Issue 4
Wild Mouse Gut Microbiota Promotes Host Fitness and Improves Disease Resistance
journal, November 2017
- Rosshart, Stephan P.; Vassallo, Brian G.; Angeletti, Davide
- Cell, Vol. 171, Issue 5
Distribution of Bacteria Influential on the Development andthe Decay of Gymnodinium nagasakiense Red Tide and Their Effects on Algal Growth.
journal, January 1991
- Fukami, Kimio; Nishijima, Toshitaka; Murata, Hiroshi
- NIPPON SUISAN GAKKAISHI, Vol. 57, Issue 12
Climate-smart soils
journal, April 2016
- Paustian, Keith; Lehmann, Johannes; Ogle, Stephen
- Nature, Vol. 532, Issue 7597
Competition and Coexistence: The Effects of Resource Transport and Supply Rates
journal, December 1994
- Huston, Michael A.; DeAngelis, Donald L.
- The American Naturalist, Vol. 144, Issue 6
Cospeciation of gut microbiota with hominids
journal, July 2016
- Moeller, A. H.; Caro-Quintero, A.; Mjungu, D.
- Science, Vol. 353, Issue 6297
Building the crops of tomorrow: advantages of symbiont-based approaches to improving abiotic stress tolerance
journal, June 2014
- Coleman-Derr, Devin; Tringe, Susannah G.
- Frontiers in Microbiology, Vol. 5
Do nutrient-competition models predict nutrient availabilities in limnetic ecosystems?
journal, March 1997
- Leibold, Mathew A.
- Oecologia, Vol. 110, Issue 1
Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism
journal, September 2009
- Amin, S. A.; Green, D. H.; Hart, M. C.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 40
Tree genetics defines fungal partner communities that may confer drought tolerance
journal, September 2017
- Gehring, Catherine A.; Sthultz, Christopher M.; Flores-Rentería, Lluvia
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 42
Rapid responses of soil microorganisms improve plant fitness in novel environments
journal, August 2012
- Lau, J. A.; Lennon, J. T.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 35
Mechanisms of Maintenance of Species Diversity
journal, November 2000
- Chesson, Peter
- Annual Review of Ecology and Systematics, Vol. 31, Issue 1
Facultative bacterial symbionts in aphids confer resistance to parasitic wasps
journal, January 2003
- Oliver, K. M.; Russell, J. A.; Moran, N. A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 4
Insect symbionts as hidden players in insect–plant interactions
journal, December 2012
- Frago, Enric; Dicke, Marcel; Godfray, H. Charles J.
- Trends in Ecology & Evolution, Vol. 27, Issue 12
Consistency in microbiomes in cultures of Alexandrium species isolated from brackish and marine waters : Consistency in microbiomes in cultures of
journal, March 2019
- Sörenson, Eva; Bertos-Fortis, Mireia; Farnelid, Hanna
- Environmental Microbiology Reports, Vol. 11, Issue 3
A global synthesis reveals biodiversity loss as a major driver of ecosystem change
journal, May 2012
- Hooper, David U.; Adair, E. Carol; Cardinale, Bradley J.
- Nature, Vol. 486, Issue 7401
Resources: A Graphical-Mechanistic Approach to Competition and Predation
journal, September 1980
- Tilman, David
- The American Naturalist, Vol. 116, Issue 3
Exploiting diversity and synthetic biology for the production of algal biofuels
journal, August 2012
- Georgianna, D. Ryan; Mayfield, Stephen P.
- Nature, Vol. 488, Issue 7411
Defining the core Arabidopsis thaliana root microbiome
journal, August 2012
- Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera
- Nature, Vol. 488, Issue 7409
Transfer of photosynthesis genes to and from Prochlorococcus viruses
journal, July 2004
- Lindell, D.; Sullivan, M. B.; Johnson, Z. I.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
Control of Brain Development, Function, and Behavior by the Microbiome
journal, May 2015
- Sampson, Timothy R.; Mazmanian, Sarkis K.
- Cell Host & Microbe, Vol. 17, Issue 5
Inclusion of facilitation into ecological theory
journal, March 2003
- Bruno, John F.; Stachowicz, John J.; Bertness, Mark D.
- Trends in Ecology & Evolution, Vol. 18, Issue 3
Preserving microbial diversity
journal, October 2018
- Bello, Maria G. Dominguez; Knight, Rob; Gilbert, Jack A.
- Science, Vol. 362, Issue 6410
Host Plant Specialization Governed by Facultative Symbiont
journal, March 2004
- Tsuchida, T.
- Science, Vol. 303, Issue 5666
Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships
journal, May 2017
- Seymour, Justin R.; Amin, Shady A.; Raina, Jean-Baptiste
- Nature Microbiology, Vol. 2, Issue 7
A novel alphaproteobacterial ectosymbiont promotes the growth of the hydrocarbon-rich green alga Botryococcus braunii
journal, July 2015
- Tanabe, Yuuhiko; Okazaki, Yusuke; Yoshida, Masaki
- Scientific Reports, Vol. 5, Issue 1
Diatom-Bacteria Interactions Modulate the Composition and Productivity of Benthic Diatom Biofilms
journal, June 2019
- Koedooder, Coco; Stock, Willem; Willems, Anne
- Frontiers in Microbiology, Vol. 10
Microbiota Modulate Behavioral and Physiological Abnormalities Associated with Neurodevelopmental Disorders
journal, December 2013
- Hsiao, Elaine Y.; McBride, Sara W.; Hsien, Sophia
- Cell, Vol. 155, Issue 7
Industrial-strength ecology: trade-offs and opportunities in algal biofuel production
journal, September 2013
- Shurin, Jonathan B.; Abbott, Rachel L.; Deal, Michael S.
- Ecology Letters, Vol. 16, Issue 11
COMBO: a defined freshwater culture medium for algae and zooplankton
journal, January 1998
- Kilham, Susan S.; Kreeger, Daniel A.; Lynn, Scott G.
- Hydrobiologia, Vol. 377, Issue 1/3, p. 147-159
The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level
journal, December 2007
- Litchman, Elena; Klausmeier, Christopher A.; Schofield, Oscar M.
- Ecology Letters, Vol. 10, Issue 12
Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton
journal, May 2004
- Klausmeier, Christopher A.; Litchman, Elena; Daufresne, Tanguy
- Nature, Vol. 429, Issue 6988
The Influence of Functional Diversity and Composition on Ecosystem Processes
journal, August 1997
- Tilman, D.
- Science, Vol. 277, Issue 5330
Experimental evidence that evolutionary relatedness does not affect the ecological mechanisms of coexistence in freshwater green algae
journal, September 2013
- Narwani, Anita; Alexandrou, Markos A.; Oakley, Todd H.
- Ecology Letters, Vol. 16, Issue 11
Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa
journal, August 2019
- Jackrel, Sara L.; White, Jeffrey D.; Evans, Jacob T.
- Molecular Ecology, Vol. 28, Issue 17
Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome
journal, June 2014
- Shi, Weibing; Moon, Christina D.; Leahy, Sinead C.
- Genome Research, Vol. 24, Issue 9
Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use
journal, April 2012
- Kleiner, M.; Wentrup, C.; Lott, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
Plant endophytes and arbuscular mycorrhizal fungi alter plant competition
journal, April 2018
- Zhou, Yong; Li, Xia; Gao, Yuan
- Functional Ecology, Vol. 32, Issue 5
Niche and fitness differences relate the maintenance of diversity to ecosystem function
journal, May 2011
- Carroll, Ian T.; Cardinale, Bradley J.; Nisbet, Roger M.
- Ecology, Vol. 92, Issue 5
Antagonistic association of the chlorellavorus bacterium (“Bdellovibrio” chlorellavorus) withChlorella vulgaris
journal, January 1978
- Coder, David M.; Starr, Mortimer P.
- Current Microbiology, Vol. 1, Issue 1
Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator
journal, June 2017
- Ajjawi, Imad; Verruto, John; Aqui, Moena
- Nature Biotechnology, Vol. 35, Issue 7
Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities
journal, November 2013
- Hanshew, Alissa S.; Mason, Charles J.; Raffa, Kenneth F.
- Journal of Microbiological Methods, Vol. 95, Issue 2
Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge
journal, July 2015
- Bertrand, Erin M.; McCrow, John P.; Moustafa, Ahmed
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 32
Diversity of locust gut bacteria protects against pathogen invasion
journal, December 2005
- Dillon, R. J.; Vennard, C. T.; Buckling, A.
- Ecology Letters, Vol. 8, Issue 12
Biodiversity improves the ecological design of sustainable biofuel systems
journal, June 2018
- Godwin, Casey M.; Lashaway, Aubrey R.; Hietala, David C.
- GCB Bioenergy, Vol. 10, Issue 10
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998
- Field, C. B.
- Science, Vol. 281, Issue 5374
Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions
journal, October 2018
- Samo, Ty J.; Kimbrel, Jeffrey A.; Nilson, Daniel J.
- Environmental Microbiology, Vol. 20, Issue 12
Novel approach for the development of axenic microalgal cultures from environmental samples
journal, July 2013
- Cho, Dae-Hyun; Ramanan, Rishiram; Kim, Byung-Hyuk
- Journal of Phycology, Vol. 49, Issue 4
PPFMs and other Covert Contaminants: Is There More to Plant Physiology than just Plant?
journal, January 1994
- Holland, M.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 45, Issue 1
Genetic regulation of biological nitrogen fixation
journal, August 2004
- Dixon, Ray; Kahn, Daniel
- Nature Reviews Microbiology, Vol. 2, Issue 8
Isolation and Properties of a Bacterium Inhibiting the Growth of Gymnodinium nagasakiense
journal, January 1992
- Fukami, Kimio; Yuzawa, Atsushi; Nishijima, Toshitaka
- NIPPON SUISAN GAKKAISHI, Vol. 58, Issue 6
Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria
journal, May 2015
- Amin, S. A.; Hmelo, L. R.; van Tol, H. M.
- Nature, Vol. 522, Issue 7554
Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior
journal, January 2013
- Badri, Dayakar V.; Zolla, Gaston; Bakker, Matthew G.
- New Phytologist, Vol. 198, Issue 1
The Evolution of Modern Eukaryotic Phytoplankton
journal, July 2004
- Falkowski, P. G.
- Science, Vol. 305, Issue 5682
Phytoplankton exudation: exploitation of the microbial loop as a defence against algal viruses
journal, January 1995
- Murray, Alexander G.
- Journal of Plankton Research, Vol. 17, Issue 5
The human microbiome: at the interface of health and disease
journal, March 2012
- Cho, Ilseung; Blaser, Martin J.
- Nature Reviews Genetics, Vol. 13, Issue 4
Diversity and heritability of the maize rhizosphere microbiome under field conditions
journal, April 2013
- Peiffer, J. A.; Spor, A.; Koren, O.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 16
Microplate-based high throughput screening procedure for the isolation of lipid-rich marine microalgae
journal, January 2011
- Pereira, Hugo; Barreira, Luísa; Mozes, André
- Biotechnology for Biofuels, Vol. 4, Issue 1
A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment
journal, July 2015
- van der Heijden, Marcel GA; Bruin, Susanne de; Luckerhoff, Ludo
- The ISME Journal, Vol. 10, Issue 2
Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota
journal, August 2013
- Sison-Mangus, Marilou P.; Jiang, Sunny; Tran, Kevin N.
- The ISME Journal, Vol. 8, Issue 1
Algae acquire vitamin B12 through a symbiotic relationship with bacteria
journal, November 2005
- Croft, Martin T.; Lawrence, Andrew D.; Raux-Deery, Evelyne
- Nature, Vol. 438, Issue 7064
Community structure follows simple assembly rules in microbial microcosms
journal, March 2017
- Friedman, Jonathan; Higgins, Logan M.; Gore, Jeff
- Nature Ecology & Evolution, Vol. 1, Issue 5
Mechanisms of Coexistence in Competitive Metacommunities
journal, January 2004
- Amarasekare,
- The American Naturalist, Vol. 164, Issue 3
Ecological implications of cyanobacterial toxins in aquatic food webs
journal, November 1996
- Christoffersen, Kirsten
- Phycologia, Vol. 35, Issue sup6
Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria
journal, January 2016
- Smriga, Steven; Fernandez, Vicente I.; Mitchell, James G.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 6
Mycorrhizal fungal identity and diversity relaxes plant–plant competition
journal, June 2011
- Wagg, Cameron; Jansa, Jan; Stadler, Marina
- Ecology, Vol. 92, Issue 6
Rethinking heritability of the microbiome
journal, September 2015
- Opstal, Edward J. van; Bordenstein, Seth R.
- Science, Vol. 349, Issue 6253
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.