Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria
Abstract
Abstract Recent studies have highlighted the capacity of marine diatoms at the foundation of ocean food webs and biogeochemical cycles to respond to environmental change. These responses are a combination of physiological acclimation and evolutionary responses. The latter occur rapidly within a few hundred generations (translating to a scale of months to years), due to the large standing genetic variation and short generation times of diatom populations. Studies are usually carried out on diatom species in their planktonic state, but this may constitute a stark oversimplification: diatoms readily form biofilms in the water column of shallow coastal areas, where biofilm formation affects carbon export, and in the benthos, where biofilms contribute significantly to sediment stability. Here, I have carried out a 400‐generation selection experiment, where I evolved the diatom Thalassiosira pseudonana and its associated bacteria. Bacteria and diatom were cultured in their planktonic form, and under strong selection for rapid biofilm formation in temperature and nutrient regimes differing in their severity and stability. I find that biofilm formation is enhanced under mild warming and rapid thermal fluctuations but not under extreme warming regardless of nutrient availability. Evolutionary responses are slower in biofilms under benign conditions but speed up under extrememore »
- Authors:
-
[1]
- Centre for Earth Systems and Sustainability Research/Institute of Marine ecosystem and Fisheries Science (CEN/IMF) University of Hamburg Hamburg Germany, Environment and Sustainability Institute University of Exeter Exeter UK
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1474203
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Limnology and Oceanography
- Additional Journal Information:
- Journal Name: Limnology and Oceanography Journal Volume: 64 Journal Issue: 2; Journal ID: ISSN 0024-3590
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Schaum, C. ‐E. Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria. United States: N. p., 2018.
Web. doi:10.1002/lno.11050.
Schaum, C. ‐E. Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria. United States. https://doi.org/10.1002/lno.11050
Schaum, C. ‐E. Thu .
"Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria". United States. https://doi.org/10.1002/lno.11050.
@article{osti_1474203,
title = {Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria},
author = {Schaum, C. ‐E.},
abstractNote = {Abstract Recent studies have highlighted the capacity of marine diatoms at the foundation of ocean food webs and biogeochemical cycles to respond to environmental change. These responses are a combination of physiological acclimation and evolutionary responses. The latter occur rapidly within a few hundred generations (translating to a scale of months to years), due to the large standing genetic variation and short generation times of diatom populations. Studies are usually carried out on diatom species in their planktonic state, but this may constitute a stark oversimplification: diatoms readily form biofilms in the water column of shallow coastal areas, where biofilm formation affects carbon export, and in the benthos, where biofilms contribute significantly to sediment stability. Here, I have carried out a 400‐generation selection experiment, where I evolved the diatom Thalassiosira pseudonana and its associated bacteria. Bacteria and diatom were cultured in their planktonic form, and under strong selection for rapid biofilm formation in temperature and nutrient regimes differing in their severity and stability. I find that biofilm formation is enhanced under mild warming and rapid thermal fluctuations but not under extreme warming regardless of nutrient availability. Evolutionary responses are slower in biofilms under benign conditions but speed up under extreme and fluctuating conditions. Taxonomic composition of the associated bacteria is driven by the temperature selection regime in biofilms but not in planktonic samples. I also show that T. pseudonana , when selected for biofilm formation, presents predictable and sequential morphologies that are not usually observed in planktonic T. pseudonana.},
doi = {10.1002/lno.11050},
journal = {Limnology and Oceanography},
number = 2,
volume = 64,
place = {United States},
year = {Thu Sep 27 00:00:00 EDT 2018},
month = {Thu Sep 27 00:00:00 EDT 2018}
}
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Works referenced in this record:
Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review
journal, March 2018
- Boyd, Philip W.; Collins, Sinead; Dupont, Sam
- Global Change Biology, Vol. 24, Issue 6
Phenotypic Plasticity Facilitates Mutational Variance, Genetic Variance, and Evolvability Along the Major axis of Environmental Variation: Phenotypic Plasticity Facilitates Mutational Variance, Genetic Variance, and Evolvability
journal, May 2012
- Draghi, Jeremy A.; Whitlock, Michael C.
- Evolution, Vol. 66, Issue 9
Evolutionary potential of marine phytoplankton under ocean acidification
journal, November 2013
- Collins, Sinéad; Rost, Björn; Rynearson, Tatiana A.
- Evolutionary Applications, Vol. 7, Issue 1
Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols
journal, July 2011
- Zimmermann, Jonas; Jahn, Regine; Gemeinholzer, Birgit
- Organisms Diversity & Evolution, Vol. 11, Issue 3
A tortoise–hare pattern seen in adapting structured and unstructured populations suggests a rugged fitness landscape in bacteria
journal, May 2015
- Nahum, Joshua R.; Godfrey-Smith, Peter; Harding, Brittany N.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 24
Plasticity predicts evolution in a marine alga
journal, October 2014
- Schaum, C. Elisa; Collins, Sinéad
- Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1793
Response of a coastal tropical pelagic microbial community to changing salinity and temperature
journal, June 2016
- Kaur-Kahlon, G.; Kumar, S.; Rehnstam-Holm, As
- Aquatic Microbial Ecology, Vol. 77, Issue 1
Adaptive radiation in a heterogeneous environment
journal, July 1998
- Rainey, Paul B.; Travisano, Michael
- Nature, Vol. 394, Issue 6688
Species Interactions Alter Evolutionary Responses to a Novel Environment
journal, May 2012
- Lawrence, Diane; Fiegna, Francesca; Behrends, Volker
- PLoS Biology, Vol. 10, Issue 5
Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change
journal, December 2012
- Boyd, Pw; Hutchins, Da
- Marine Ecology Progress Series, Vol. 470
Diatoms favor their younger daughters
journal, August 2012
- Laney, Samuel R.; Olson, Robert J.; Sosik, Heidi M.
- Limnology and Oceanography, Vol. 57, Issue 5
Ubiquitous marine bacterium inhibits diatom cell division
journal, September 2016
- van Tol, Helena M.; Amin, Shady A.; Armbrust, E. Virginia
- The ISME Journal, Vol. 11, Issue 1
The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism
journal, October 2004
- Armbrust, E. V.
- Science, Vol. 306, Issue 5693
The Effect of Immigration on the Adaptation of Microbial Communities to Warming
journal, February 2016
- Lawrence, Diane; Bell, Thomas; Barraclough, Timothy G.
- The American Naturalist, Vol. 187, Issue 2
Transparent exopolymer particles (TEP): A critical factor in aquatic biofilm initiation and fouling on filtration membranes
journal, August 2011
- Berman, Tom; Mizrahi, Roi; Dosoretz, Carlos G.
- Desalination, Vol. 276, Issue 1-3
Interspecies Interactions within Oral Microbial Communities
journal, December 2007
- Kuramitsu, H. K.; He, X.; Lux, R.
- Microbiology and Molecular Biology Reviews, Vol. 71, Issue 4
Resource Availability and Competition Shape the Evolution of Survival and Growth Ability in a Bacterial Community
journal, September 2013
- Pekkonen, Minna; Ketola, Tarmo; Laakso, Jouni T.
- PLoS ONE, Vol. 8, Issue 9
Diatom teratological forms and environmental alterations: a review
journal, January 2009
- Falasco, Elisa; Bona, Francesca; Badino, Guido
- Hydrobiologia, Vol. 623, Issue 1
The Response of Thalassiosira pseudonana to Long-Term Exposure to Increased CO2 and Decreased pH
journal, October 2011
- Crawfurd, Katharine J.; Raven, John A.; Wheeler, Glen L.
- PLoS ONE, Vol. 6, Issue 10
Competition limits adaptation and productivity in a photosynthetic alga at elevated CO 2
journal, July 2010
- Collins, Sinéad
- Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1703
Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity
journal, August 2012
- Yang, Guiyuan; Gao, Kunshan
- Marine Environmental Research, Vol. 79
Toward a General Theory of Adaptive Radiation: Insights from Microbial Experimental Evolution
journal, June 2009
- Kassen, Rees
- Annals of the New York Academy of Sciences, Vol. 1168, Issue 1
Environmental harshness is positively correlated with intraspecific divergence in mammals and birds
journal, November 2013
- Botero, Carlos A.; Dor, Roi; McCain, Christy M.
- Molecular Ecology, Vol. 23, Issue 2
Thermal Performance Curves of Functional Traits Aid Understanding of Thermally Induced Changes in Diatom-Mediated Biogeochemical Fluxes
journal, April 2016
- Baker, Kirralee G.; Robinson, Charlotte M.; Radford, Dale T.
- Frontiers in Marine Science, Vol. 3
Real-time microbial adaptive diversification in soil
journal, February 2013
- Gómez, Pedro; Buckling, Angus
- Ecology Letters, Vol. 16, Issue 5
Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae
journal, November 2005
- Matz, C.; McDougald, D.; Moreno, A. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 46
Ecological succession in long-term experimentally evolved biofilms produces synergistic communities
journal, September 2010
- Poltak, Steffen R.; Cooper, Vaughn S.
- The ISME Journal, Vol. 5, Issue 3
Antagonistic coevolution limits population persistence of a virus in a thermally deteriorating environment: Coevolution limits evolutionary rescue
journal, January 2011
- Zhang, Quan-Guo; Buckling, Angus
- Ecology Letters, Vol. 14, Issue 3
Adaptation of a globally important coccolithophore to ocean warming and acidification
journal, September 2014
- Schlüter, Lothar; Lohbeck, Kai T.; Gutowska, Magdalena A.
- Nature Climate Change, Vol. 4, Issue 11
Interactions between Diatoms and Bacteria
journal, August 2012
- Amin, S. A.; Parker, M. S.; Armbrust, E. V.
- Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3
Algae–bacteria interactions: Evolution, ecology and emerging applications
journal, January 2016
- Ramanan, Rishiram; Kim, Byung-Hyuk; Cho, Dae-Hyun
- Biotechnology Advances, Vol. 34, Issue 1
Temperature-nutrient interactions exacerbate sensitivity to warming in phytoplankton
journal, March 2017
- Thomas, Mridul K.; Aranguren-Gassis, María; Kremer, Colin T.
- Global Change Biology, Vol. 23, Issue 8
Characterization of Extracellular RNAs Produced by the Marine Photosynthetic Bacterium Rhodovulum sulfidophilum
journal, April 2006
- Ando, Tomoaki; Suzuki, Hiromichi; Nishimura, Seiichiro
- The Journal of Biochemistry, Vol. 139, Issue 4
Experimental evolution gone wild
journal, May 2015
- Scheinin, M.; Riebesell, U.; Rynearson, T. A.
- Journal of The Royal Society Interface, Vol. 12, Issue 106
Facilitation as Attenuating of Environmental Stress among Structured Microbial Populations
journal, January 2016
- Silveira Martins, Suzana Cláudia; Santaella, Sandra Tédde; Martins, Claudia Miranda
- The Scientific World Journal, Vol. 2016
Elevated temperature alters proteomic responses of individual organisms within a biofilm community
journal, July 2014
- Mosier, Annika C.; Li, Zhou; Thomas, Brian C.
- The ISME Journal, Vol. 9, Issue 1
The interconnection between biofilm formation and horizontal gene transfer
journal, July 2012
- Madsen, Jonas Stenløkke; Burmølle, Mette; Hansen, Lars Hestbjerg
- FEMS Immunology & Medical Microbiology, Vol. 65, Issue 2
Character Displacement Promotes Cooperation in Bacterial Biofilms
journal, October 2006
- Brockhurst, Michael A.; Hochberg, Michael E.; Bell, Thomas
- Current Biology, Vol. 16, Issue 20
Mixed-Effects Models in Sand S-PLUS
book, January 2000
- Pinheiro, José C.; Bates, Douglas M.
- Statistics and Computing
Dynamic approaches of mixed species biofilm formation using modern technologies
journal, July 2012
- Doiron, Kim; Linossier, Isabelle; Fay, Fabienne
- Marine Environmental Research, Vol. 78
Evolution of phenotypic plasticity in extreme environments
journal, May 2017
- Chevin, Luis-Miguel; Hoffmann, Ary A.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1723
The production of dissolved organic matter by phytoplankton and its importance to bacteria: Patterns across marine and freshwater systems
journal, September 1991
- Baines, Stephen B.; Pace, Michael L.
- Limnology and Oceanography, Vol. 36, Issue 6
Evolutionary tipping points in the capacity to adapt to environmental change
journal, November 2014
- Botero, Carlos A.; Weissing, Franz J.; Wright, Jonathan
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 1
Antagonistic coevolution accelerates molecular evolution
journal, February 2010
- Paterson, Steve; Vogwill, Tom; Buckling, Angus
- Nature, Vol. 464, Issue 7286
Effects of phytoplankton community on production, size, and export of large aggregates: A world-ocean analysis
journal, August 2009
- Guidi, Lionel; Stemmann, Lars; Jackson, George A.
- Limnology and Oceanography, Vol. 54, Issue 6
Polysaccharide aggregation as a potential sink of marine dissolved organic carbon
journal, April 2004
- Engel, Anja; Thoms, Silke; Riebesell, Ulf
- Nature, Vol. 428, Issue 6986
Division of Labor, Bet Hedging, and the Evolution of Mixed Biofilm Investment Strategies
journal, August 2017
- Lowery, Nick Vallespir; McNally, Luke; Ratcliff, William C.
- mBio, Vol. 8, Issue 4
SHORT- VERSUS LONG-TERM RESPONSES TO CHANGING CO 2 IN A COASTAL DINOFLAGELLATE BLOOM: IMPLICATIONS FOR INTERSPECIFIC COMPETITIVE INTERACTIONS AND COMMUNITY STRUCTURE
journal, January 2013
- Tatters, Avery O.; Schnetzer, Astrid; Fu, Feixue
- Evolution, Vol. 67, Issue 7
Chlorophyll a Determination: Improvements in Methodology
journal, January 1978
- Holm-Hansen, Osmund; Riemann, Bo
- Oikos, Vol. 30, Issue 3
Theoretical Predictions for How Temperature Affects the Dynamics of Interacting Herbivores and Plants
journal, November 2011
- O’Connor, Mary I.; Gilbert, Benjamin; Brown, Christopher J.
- The American Naturalist, Vol. 178, Issue 5
Evolution of bacterial life-history traits is sensitive to community structure
journal, June 2016
- Ketola, Tarmo; Mikonranta, Lauri; Mappes, Johanna
- Evolution, Vol. 70, Issue 6
Warming and Ocean Acidification Effects on Phytoplankton—From Species Shifts to Size Shifts within Species in a Mesocosm Experiment
journal, May 2015
- Sommer, Ulrich; Paul, Carolin; Moustaka-Gouni, Maria
- PLOS ONE, Vol. 10, Issue 5
Biofilm and capsule formation of the diatom Achnanthidium minutissimum are affected by a bacterium
journal, March 2015
- Windler, Miriam; Leinweber, Katrin; Bartulos, Carolina Rio
- Journal of Phycology, Vol. 51, Issue 2
Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis
journal, March 2017
- Schaum, C. -Elisa; Barton, Samuel; Bestion, Elvire
- Nature Ecology & Evolution, Vol. 1, Issue 4
Five Years of Experimental Warming Increases the Biodiversity and Productivity of Phytoplankton
journal, December 2015
- Yvon-Durocher, Gabriel; Allen, Andrew P.; Cellamare, Maria
- PLOS Biology, Vol. 13, Issue 12
Quantitative proteomics of a B 12 -dependent alga grown in coculture with bacteria reveals metabolic tradeoffs required for mutualism
journal, October 2017
- Helliwell, Katherine E.; Pandhal, Jagroop; Cooper, Matthew B.
- New Phytologist, Vol. 217, Issue 2
Experimental evolution in biofilm populations
journal, February 2016
- Steenackers, Hans P.; Parijs, Ilse; Foster, Kevin R.
- FEMS Microbiology Reviews, Vol. 40, Issue 3
Biofilm formation at warming temperature: acceleration of microbial colonization and microbial interactive effects
journal, November 2010
- Villanueva, Verónica Díaz; Font, Jordi; Schwartz, Thomas
- Biofouling, Vol. 27, Issue 1
Temporal changes in species interactions in simple aquatic bacterial communities
journal, January 2012
- Pekkonen, Minna; Laakso, Jouni T.
- BMC Ecology, Vol. 12, Issue 1
Rapid isolation of high molecular weight plant DNA
journal, January 1980
- Murray, M. G.; Thompson, W. F.
- Nucleic Acids Research, Vol. 8, Issue 19
Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton
journal, November 2015
- Padfield, Daniel; Yvon-Durocher, Genevieve; Buckling, Angus
- Ecology Letters, Vol. 19, Issue 2
Primary Production of the Biosphere: Integrating Terrestrial and Oceanic Components
journal, July 1998
- Field, C. B.
- Science, Vol. 281, Issue 5374
Evolutionary consequences of multidriver environmental change in an aquatic primary producer
journal, August 2017
- Brennan, Georgina L.; Colegrave, Nick; Collins, Sinéad
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
Biofilm Formation As a Response to Ecological Competition
journal, July 2015
- Oliveira, Nuno M.; Martinez-Garcia, Esteban; Xavier, Joao
- PLOS Biology, Vol. 13, Issue 7
Quantitative Genetics of Continuous Reaction Norms: Thermal Sensitivity of Caterpillar Growth Rates
journal, July 2004
- Kingsolver, Joel G.; Ragland, Gregory J.; Shlichta, J. Gwen
- Evolution, Vol. 58, Issue 7
Life-history evolution in the anthropocene: effects of increasing nutrients on traits and trade-offs
journal, June 2015
- Snell-Rood, Emilie; Cothran, Rickey; Espeset, Anne
- Evolutionary Applications, Vol. 8, Issue 7
A reduced estimate of the strength of the ocean's biological carbon pump: BIOLOGICAL CARBON PUMP STRENGTH
journal, February 2011
- Henson, Stephanie A.; Sanders, Richard; Madsen, Esben
- Geophysical Research Letters, Vol. 38, Issue 4
Unexpected changes in community size structure in a natural warming experiment
journal, August 2017
- O’Gorman, Eoin J.; Zhao, Lei; Pichler, Doris E.
- Nature Climate Change, Vol. 7, Issue 9
Tradeoffs and the evolution of thermal reaction norms
journal, May 2003
- Angilletta, Michael J.; Wilson, Robbie S.; Navas, Carlos A.
- Trends in Ecology & Evolution, Vol. 18, Issue 5
Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom
journal, April 2018
- Schaum, C. -Elisa; Buckling, A.; Smirnoff, N.
- Nature Communications, Vol. 9, Issue 1
The Stabilisation Potential of Individual and Mixed Assemblages of Natural Bacteria and Microalgae
journal, November 2010
- Lubarsky, Helen V.; Hubas, Cédric; Chocholek, Melanie
- PLoS ONE, Vol. 5, Issue 11
Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation
journal, June 2003
- Elena, Santiago F.; Lenski, Richard E.
- Nature Reviews Genetics, Vol. 4, Issue 6
Evolution of cooperation and conflict in experimental bacterial populations
journal, September 2003
- Rainey, Paul B.; Rainey, Katrina
- Nature, Vol. 425, Issue 6953
Warming alters the metabolic balance of ecosystems
journal, July 2010
- Yvon-Durocher, Gabriel; Jones, J. Iwan; Trimmer, Mark
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1549
Habitat diversity and ecosystem multifunctionality—The importance of direct and indirect effects
journal, February 2017
- Alsterberg, Christian; Roger, Fabian; Sundbäck, Kristina
- Science Advances, Vol. 3, Issue 2
Biogenic Stabilization of Intertidal Sediments: The Importance of Extracellular Polymeric Substances Produced by Benthic Diatoms
journal, May 2005
- de Brouwer, J. F. C.; Wolfstein, K.; Ruddy, G. K.
- Microbial Ecology, Vol. 49, Issue 4
Eukaryotic plankton diversity in the sunlit ocean
journal, May 2015
- de Vargas, C.; Audic, S.; Henry, N.
- Science, Vol. 348, Issue 6237
The life of diatoms in the world's oceans
journal, May 2009
- Armbrust, E. Virginia
- Nature, Vol. 459, Issue 7244
Sinking phytoplankton associated with carbon flux in the Atlantic Ocean: Sinking phytoplankton and carbon flux
journal, May 2016
- Durkin, Colleen A.; Van Mooy, Benjamin A. S.; Dyhrman, Sonya T.
- Limnology and Oceanography, Vol. 61, Issue 4
Biogeochemical Controls and Feedbacks on Ocean Primary Production
journal, July 1998
- Falkowski, P. G.
- Science, Vol. 281, Issue 5374
Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii
journal, May 2005
- Rynearson, Tatiana A.; Armbrust, E. Virginia
- Molecular Ecology, Vol. 14, Issue 6
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens . II. Role of the GGDEF Regulator WspR in Evolution and Development of the Wrinkly Spreader Phenotype
journal, April 2006
- Goymer, Patrick; Kahn, Sophie G.; Malone, Jacob G.
- Genetics, Vol. 173, Issue 2
Motility of Non-Raphid Diatoms
journal, November 2006
- Sato, Shinya; Medlin, Linda K.
- Diatom Research, Vol. 21, Issue 2
Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions
journal, December 2008
- Rost, B.; Zondervan, I.; Wolf-Gladrow, D.
- Marine Ecology Progress Series, Vol. 373
Interactions of bacteria with diatoms: influence on natural marine biofilms
journal, August 2013
- Khandeparker, Lidita; D'Costa, Priya M.; Anil, Arga C.
- Marine Ecology, Vol. 35, Issue 2