Quantifying the local adaptive landscape of a nascent bacterial community

Ascensao, Joao A.; Wetmore, Kelly M.; Good, Benjamin H.; Arkin, Adam P.; Hallatschek, Oskar

doi:10.1038/s41467-022-35677-5

Title: Quantifying the local adaptive landscape of a nascent bacterial community

Journal Article · 15 January 2023 · Nature Communications

DOI: https://doi.org/10.1038/s41467-022-35677-5 · OSTI ID:1909251

; Wetmore, Kelly M.;

;

Abstract The fitness effects of all possible mutations available to an organism largely shape the dynamics of evolutionary adaptation. Yet, whether and how this adaptive landscape changes over evolutionary times, especially upon ecological diversification and changes in community composition, remains poorly understood. We sought to fill this gap by analyzing a stable community of two closely related ecotypes (“L” and “S”) shortly after they emerged within the E. coli Long-Term Evolution Experiment (LTEE). We engineered genome-wide barcoded transposon libraries to measure the invasion fitness effects of all possible gene knockouts in the coexisting strains as well as their ancestor, for many different, ecologically relevant conditions. We find consistent statistical patterns of fitness effect variation across both genetic background and community composition, despite the idiosyncratic behavior of individual knockouts. Additionally, fitness effects are correlated with evolutionary outcomes for a number of conditions, possibly revealing shifting patterns of adaptation. Together, our results reveal how ecological and epistatic effects combine to shape the adaptive landscape in a nascent ecological community.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1909251

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (69)

Fluid Communities: A Competitive, Scalable and Diverse Community Detection Algorithm Parés, Ferran; Gasulla, Dario Garcia; Vilalta, Armand Complex Networks & Their Applications VI https://doi.org/10.1007/978-3-319-72150-7_19	book	November 2017
Long-Term Experimental Evolution in Escherichia coli. XIII. Phylogenetic History of a Balanced Polymorphism Rozen, Daniel E.; Schneider, Dominique; Lenski, Richard E. Journal of Molecular Evolution, Vol. 61, Issue 2 https://doi.org/10.1007/s00239-004-0322-2	journal	June 2005
Bayesian point null hypothesis testing via the posterior likelihood ratio Aitkin, Murray; Boys, Richard J.; Chadwick, Tom Statistics and Computing, Vol. 15, Issue 3 https://doi.org/10.1007/s11222-005-1310-0	journal	July 2005
Development of a Comprehensive Genotype-to-Fitness Map of Adaptation-Driving Mutations in Yeast Venkataram, Sandeep; Dunn, Barbara; Li, Yuping Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.002	journal	September 2016
Adaptive Evolution within Gut Microbiomes of Healthy People Zhao, Shijie; Lieberman, Tami D.; Poyet, Mathilde Cell Host & Microbe, Vol. 25, Issue 5 https://doi.org/10.1016/j.chom.2019.03.007	journal	May 2019
Quantifying rapid bacterial evolution and transmission within the mouse intestine Vasquez, Kimberly S.; Willis, Lisa; Cira, Nate J. Cell Host & Microbe, Vol. 29, Issue 9 https://doi.org/10.1016/j.chom.2021.08.003	journal	September 2021
The Speed of Evolution and Maintenance of Variation in Asexual Populations Desai, Michael M.; Fisher, Daniel S.; Murray, Andrew W. Current Biology, Vol. 17, Issue 5 https://doi.org/10.1016/j.cub.2007.01.072	journal	March 2007
Hidden Complexity of Yeast Adaptation under Simple Evolutionary Conditions Li, Yuping; Venkataram, Sandeep; Agarwala, Atish Current Biology, Vol. 28, Issue 4 https://doi.org/10.1016/j.cub.2018.01.009	journal	February 2018
Evolution of high mutation rates in experimental populations of E. coli Sniegowski, Paul D.; Gerrish, Philip J.; Lenski, Richard E. Nature, Vol. 387, Issue 6634 https://doi.org/10.1038/42701	journal	June 1997
Quantitative evolutionary dynamics using high-resolution lineage tracking Levy, Sasha F.; Blundell, Jamie R.; Venkataram, Sandeep Nature, Vol. 519, Issue 7542 https://doi.org/10.1038/nature14279	journal	February 2015
Tempo and mode of genome evolution in a 50,000-generation experiment Tenaillon, Olivier; Barrick, Jeffrey E.; Ribeck, Noah Nature, Vol. 536, Issue 7615 https://doi.org/10.1038/nature18959	journal	August 2016
The dynamics of molecular evolution over 60,000 generations Good, Benjamin H.; McDonald, Michael J.; Barrick, Jeffrey E. Nature, Vol. 551, Issue 7678 https://doi.org/10.1038/nature24287	journal	October 2017
Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective Folkesson, Anders; Jelsbak, Lars; Yang, Lei Nature Reviews Microbiology, Vol. 10, Issue 12 https://doi.org/10.1038/nrmicro2907	journal	November 2012
Prochlorococcus: the structure and function of collective diversity Biller, Steven J.; Berube, Paul M.; Lindell, Debbie Nature Reviews Microbiology, Vol. 13, Issue 1 https://doi.org/10.1038/nrmicro3378	journal	December 2014
The dynamics of adaptive genetic diversity during the early stages of clonal evolution Blundell, Jamie R.; Schwartz, Katja; Francois, Danielle Nature Ecology & Evolution, Vol. 3, Issue 2 https://doi.org/10.1038/s41559-018-0758-1	journal	December 2018
Single nucleotide mapping of trait space reveals Pareto fronts that constrain adaptation Li, Yuping; Petrov, Dmitri A.; Sherlock, Gavin Nature Ecology & Evolution, Vol. 3, Issue 11 https://doi.org/10.1038/s41559-019-0993-0	journal	October 2019
Mutualism-enhancing mutations dominate early adaptation in a two-species microbial community Venkataram, Sandeep; Kuo, Huan-Yu; Hom, Erik F. Y. Nature Ecology & Evolution, Vol. 7, Issue 1 https://doi.org/10.1038/s41559-022-01923-8	journal	January 2023
Renewing Felsenstein’s phylogenetic bootstrap in the era of big data Lemoine, F.; Domelevo Entfellner, J. -B.; Wilkinson, E. Nature, Vol. 556, Issue 7702 https://doi.org/10.1038/s41586-018-0043-0	journal	April 2018
Mutant phenotypes for thousands of bacterial genes of unknown function Price, Morgan N.; Wetmore, Kelly M.; Waters, R. Jordan Nature, Vol. 557, Issue 7706 https://doi.org/10.1038/s41586-018-0124-0	journal	May 2018
High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast Nguyen Ba, Alex N.; Cvijović, Ivana; Rojas Echenique, José I. Nature, Vol. 575, Issue 7783 https://doi.org/10.1038/s41586-019-1749-3	journal	November 2019
GOATOOLS: A Python library for Gene Ontology analyses Klopfenstein, D. V.; Zhang, Liangsheng; Pedersen, Brent S. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-28948-z	journal	July 2018
Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli Blount, Z. D.; Borland, C. Z.; Lenski, R. E. Proceedings of the National Academy of Sciences, Vol. 105, Issue 23 https://doi.org/10.1073/pnas.0803151105	journal	June 2008
Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations Good, B. H.; Rouzine, I. M.; Balick, D. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 13 https://doi.org/10.1073/pnas.1119910109	journal	February 2012
Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations Frenkel, Evgeni M.; McDonald, Michael J.; Van Dyken, J. David Proceedings of the National Academy of Sciences, Vol. 112, Issue 36 https://doi.org/10.1073/pnas.1506184112	journal	August 2015
Adaptation limits ecological diversification and promotes ecological tinkering during the competition for substitutable resources Good, Benjamin H.; Martis, Stephen; Hallatschek, Oskar Proceedings of the National Academy of Sciences, Vol. 115, Issue 44 https://doi.org/10.1073/pnas.1807530115	journal	October 2018
Evolutionary consequences of niche construction and their implications for ecology Laland, K. N.; Odling-Smee, F. J.; Feldman, M. W. Proceedings of the National Academy of Sciences, Vol. 96, Issue 18 https://doi.org/10.1073/pnas.96.18.10242	journal	August 1999
A Third Bacterial System for the Assembly of Iron-Sulfur Clusters with Homologs in Archaea and Plastids Takahashi, Yasuhiro; Tokumoto, Umechiyo Journal of Biological Chemistry, Vol. 277, Issue 32 https://doi.org/10.1074/jbc.C200365200	journal	June 2002
Long-Term Experimental Evolution in Escherichia coli. II. Changes in Life-History Traits During Adaptation to a Seasonal Environment Vasi, Farida; Travisano, Michael; Lenski, Richard E. The American Naturalist, Vol. 144, Issue 3 https://doi.org/10.1086/285685	journal	September 1994
Long‐Term Experimental Evolution in Escherichia coli . VIII. Dynamics of a Balanced Polymorphism Rozen, Daniel E.; Lenski, Richard E. The American Naturalist, Vol. 155, Issue 1 https://doi.org/10.1086/303299	journal	January 2000
EcoliNet: a database of cofunctional gene network for Escherichia coli Kim, Hanhae; Shim, Jung Eun; Shin, Junha Database, Vol. 2015 https://doi.org/10.1093/DATABASE/BAV001	journal	January 2015
GEOquery: a bridge between the Gene Expression Omnibus (GEO) and BioConductor Davis, S.; Meltzer, P. S. Bioinformatics, Vol. 23, Issue 14 https://doi.org/10.1093/bioinformatics/btm254	journal	May 2007
Core Genes Evolve Rapidly in the Long-Term Evolution Experiment with Escherichia coli Maddamsetti, Rohan; Hatcher, Philip J.; Green, Anna G. Genome Biology and Evolution, Vol. 9, Issue 4 https://doi.org/10.1093/gbe/evx064	journal	April 2017
Evolution of Escherichia coli During Growth in a Constant Environment Helling, Robert B.; Vargas, Christopher N.; Adams, Julian Genetics, Vol. 116, Issue 3 https://doi.org/10.1093/genetics/116.3.349	journal	July 1987
The Distribution of Fitness Effects Among Beneficial Mutations Orr, H. Allen Genetics, Vol. 163, Issue 4 https://doi.org/10.1093/genetics/163.4.1519	journal	April 2003
Recurrent Reverse Evolution Maintains Polymorphism after Strong Bottlenecks in Commensal Gut Bacteria Sousa, Ana; Ramiro, Ricardo S.; Barroso-Batista, João Molecular Biology and Evolution, Vol. 34, Issue 11 https://doi.org/10.1093/molbev/msx221	journal	August 2017
Effects of Beneficial Mutations in pykF Gene Vary over Time and across Replicate Populations in a Long-Term Experiment with Bacteria Peng, Fen; Widmann, Scott; Wünsche, Andrea Molecular Biology and Evolution, Vol. 35, Issue 1 https://doi.org/10.1093/molbev/msx279	journal	October 2017
Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play Post, David M.; Palkovacs, Eric P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1523 https://doi.org/10.1098/rstb.2009.0012	journal	June 2009
Microbial ecology of the cystic fibrosis lung Harrison, Freya. Microbiology, Vol. 153, Issue 4 https://doi.org/10.1099/mic.0.2006/004077-0	journal	April 2007
Performance of modularity maximization in practical contexts Good, Benjamin H.; de Montjoye, Yves-Alexandre; Clauset, Aaron Physical Review E, Vol. 81, Issue 4 https://doi.org/10.1103/PhysRevE.81.046106	journal	April 2010
On Modularity Clustering Brandes, U.; Delling, D.; Gaertler, M. IEEE Transactions on Knowledge and Data Engineering, Vol. 20, Issue 2 https://doi.org/10.1109/TKDE.2007.190689	journal	February 2008
Molecular signatures of resource competition: Clonal interference favors ecological diversification and can lead to incipient speciation* Amicone, Massimo; Gordo, Isabel Evolution, Vol. 75, Issue 11 https://doi.org/10.1111/EVO.14315	journal	August 2021
Death and cannibalism in a seasonal environment facilitate bacterial coexistence Rozen, Daniel E.; Philippe, Nadège; Arjan de Visser, J. Ecology Letters, Vol. 12, Issue 1 https://doi.org/10.1111/j.1461-0248.2008.01257.x	journal	January 2009
The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population Khan, A. I.; Dinh, D. M.; Schneider, D. Science, Vol. 332, Issue 6034 https://doi.org/10.1126/science.1203801	journal	June 2011
Long-Term Dynamics of Adaptation in Asexual Populations Wiser, M. J.; Ribeck, N.; Lenski, R. E. Science, Vol. 342, Issue 6164 https://doi.org/10.1126/science.1243357	journal	November 2013
Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli Plucain, J.; Hindre, T.; Le Gac, M. Science, Vol. 343, Issue 6177 https://doi.org/10.1126/science.1248688	journal	March 2014
Global epistasis makes adaptation predictable despite sequence-level stochasticity Kryazhimskiy, S.; Rice, D. P.; Jerison, E. R. Science, Vol. 344, Issue 6191 https://doi.org/10.1126/science.1250939	journal	June 2014
Higher-fitness yeast genotypes are less robust to deleterious mutations Johnson, Milo S.; Martsul, Alena; Kryazhimskiy, Sergey Science, Vol. 366, Issue 6464 https://doi.org/10.1126/science.aay4199	journal	October 2019
Idiosyncratic epistasis leads to global fitness–correlated trends Bakerlee, Christopher W.; Nguyen Ba, Alex N.; Shulgina, Yekaterina Science, Vol. 376, Issue 6593 https://doi.org/10.1126/science.abm4774	journal	May 2022
Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons Wetmore, Kelly M.; Price, Morgan N.; Waters, Robert J. mBio, Vol. 6, Issue 3, Article No. e00306-15 https://doi.org/10.1128/mBio.00306-15	journal	May 2015
Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment Großkopf, Tobias; Consuegra, Jessika; Gaffé, Joël BMC Evolutionary Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12862-016-0733-x	journal	August 2016
Equivalence between the Posterior Distribution of the Likelihood Ratio and a p-value in an Invariant Frame Smith, Isabelle; Ferrari, André Bayesian Analysis, Vol. 9, Issue 4 https://doi.org/10.1214/14-BA877	journal	December 2014
Ex Uno Plures: Clonal Reinforcement Drives Evolution of a Simple Microbial Community Kinnersley, Margie; Wenger, Jared; Kroll, Evgueny PLoS Genetics, Vol. 10, Issue 6 https://doi.org/10.1371/JOURNAL.PGEN.1004430	journal	June 2014
Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli Herron, Matthew D.; Doebeli, Michael PLoS Biology, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pbio.1001490	journal	February 2013
Evolutionary dynamics of bacteria in the gut microbiome within and across hosts Garud, Nandita R.; Good, Benjamin H.; Hallatschek, Oskar PLOS Biology, Vol. 17, Issue 1 https://doi.org/10.1371/journal.pbio.3000102	journal	January 2019
High-Throughput Identification of Adaptive Mutations in Experimentally Evolved Yeast Populations Payen, Celia; Sunshine, Anna B.; Ong, Giang T. PLOS Genetics, Vol. 12, Issue 10 https://doi.org/10.1371/journal.pgen.1006339	journal	October 2016
Beneficial Mutation–Selection Balance and the Effect of Linkage on Positive Selection Desai, Michael M.; Fisher, Daniel S. Genetics, Vol. 176, Issue 3 https://doi.org/10.1534/genetics.106.067678	journal	May 2007
The Impact of Macroscopic Epistasis on Long-Term Evolutionary Dynamics Good, Benjamin H.; Desai, Michael M. Genetics, Vol. 199, Issue 1 https://doi.org/10.1534/genetics.114.172460	journal	November 2014
The Evolutionarily Stable Distribution of Fitness Effects Rice, Daniel P.; Good, Benjamin H.; Desai, Michael M. Genetics, Vol. 200, Issue 1 https://doi.org/10.1534/genetics.114.173815	journal	March 2015
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments Smyth, Gordon K. Statistical Applications in Genetics and Molecular Biology, Vol. 3, Issue 1 https://doi.org/10.2202/1544-6115.1027	journal	January 2004
Molecular Evolution Over the Mutational Landscape Gillespie, John H. Evolution, Vol. 38, Issue 5 https://doi.org/10.2307/2408444	journal	September 1984
The Population Genetics of Adaptation: The Distribution of Factors Fixed during Adaptive Evolution Orr, H. Allen Evolution, Vol. 52, Issue 4 https://doi.org/10.2307/2411226	journal	August 1998
Statsmodels: Econometric and Statistical Modeling with Python Seabold, Skipper; Perktold, Josef Proceedings of the Python in Science Conference https://doi.org/10.25080/Majora-92bf1922-011	conference	January 2010
Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes? Graham, Emily B.; Knelman, Joseph E.; Schindlbacher, Andreas Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00214	journal	February 2016
Human Gut Microbiota: Toward an Ecology of Disease Selber-Hnatiw, Susannah; Rukundo, Belise; Ahmadi, Masoumeh Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01265	journal	July 2017
Eco-evolutionary dynamics of complex social strategies in microbial communities Harrington, Kyle I.; Sanchez, Alvaro Communicative & Integrative Biology, Vol. 7, Issue 1 https://doi.org/10.4161/cib.28230	journal	January 2014
Diversity and asynchrony in soil microbial communities stabilizes ecosystem functioning Wagg, Cameron; Hautier, Yann; Pellkofer, Sarah eLife, Vol. 10 https://doi.org/10.7554/ELIFE.62813	journal	March 2021
Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation Kinsler, Grant; Geiler-Samerotte, Kerry; Petrov, Dmitri A. eLife, Vol. 9 https://doi.org/10.7554/eLife.61271	journal	December 2020
Global epistasis emerges from a generic model of a complex trait Reddy, Gautam; Desai, Michael M. eLife, Vol. 10 https://doi.org/10.7554/eLife.64740	journal	March 2021

Similar Records

Adaptation limits ecological diversification and promotes ecological tinkering during the competition for substitutable resources

Journal Article · 2018 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1543912

Good, Benjamin H.; Martis, Stephen; Hallatschek, Oskar

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data

Journal Article · 2022 · Molecular Ecology · OSTI ID:1880160

Zhang, Yuanmeng M.; Sheikh, Sofia I.; Ward, Anna K. G.; +10 more

Modeling genome-wide enzyme evolution predicts strong epistasis underlying catalytic turnover rates

Journal Article · 2018 · Nature Communications · OSTI ID:1543751

Heckmann, David; Zielinski, Daniel C.; Palsson, Bernhard O.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
bacterial genetics
epistasis
experimental evolution
microbial ecology

Title: Quantifying the local adaptive landscape of a nascent bacterial community

Citation Formats

References (69)

Similar Records

Related Subjects