1887

Microbiology Society logo

Volume 169, Issue 8

Evolution of a cross-feeding interaction following a key innovation in a long-term evolution experiment with Open Access

Abstract

The evolution of a novel trait can profoundly change an organism’s effects on its environment, which can in turn affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following the evolution of a novel function in the Long-Term Evolution Experiment (LTEE) with . A characteristic feature of is its inability to grow aerobically on citrate (Cit). Nonetheless, a Cit variant with this capacity evolved in one LTEE population after 31 000 generations. The Cit clade then coexisted stably with another clade that retained the ancestral Cit phenotype. This coexistence was shaped by the evolution of a cross-feeding relationship based on C-dicarboxylic acids, particularly succinate, fumarate, and malate, that the Cit variants release into the medium. Both the Cit and Cit cells evolved to grow on these excreted resources. The evolution of aerobic growth on citrate thus led to a transition from an ecosystem based on a single limiting resource, glucose, to one with at least five resources that were either shared or partitioned between the two coexisting clades. Our findings show that evolutionary novelties can change environmental conditions in ways that facilitate diversity by altering ecosystem structure and the evolutionary trajectories of coexisting lineages.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): adaptation , C4-dicarboxylates , citrate , cross-feeding interaction , evolutionary tinkering and experimental evolution
Funding
This study was supported by the:
  • National Science Foundation (Award DBI-0939454)
    • Principle Award Recipient: NotApplicable
  • National Science Foundation (Award DEB-1951307)
    • Principle Award Recipient: RichardE Lenski
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001390
2023-08-31
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/8/mic001390.html?itemId=/content/journal/micro/10.1099/mic.0.001390&mimeType=html&fmt=ahah

References

  1. Darwin C. On the Origin of Species London, UK: John Murray; 1859
     [Google Scholar]
  2. Darwin C. The Formation of Vegetable Mould, Through the Action of Worms, with Observations on Their Habits London: John Murray; 1881
     [Google Scholar]
  3. Hutchinson GE. The Ecological Theater and the Evolutionary Play New Haven, CT: Yale University Press; 1965
     [Google Scholar]
  4. Dawkins R. The Extended Phenotype: The Long Reach of the Gene Oxford, UK: Oxford University Press; 1982
     [Google Scholar]
  5. Lewontin RC. The Triple Helix: Gene, Organism, and Environment Cambridge, MA: Harvard University Press; 2001
     [Google Scholar]
  6. Carroll SP, Hendry AP, Reznick DN, Fox CW. Evolution on ecological time-scales. Funct Ecol 2007; 21:387–393 [View Article]
     [Google Scholar]
  7. Matthews B, Narwani A, Hausch S, Nonaka E, Peter H et al. Toward an integration of evolutionary biology and ecosystem science. Ecol Lett 2011; 14:690–701 [View Article] [PubMed]
     [Google Scholar]
  8. Schoener TW. The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science 2011; 331:426–429 [View Article] [PubMed]
     [Google Scholar]
  9. Mayr E. Animal Species and Evolution Cambridge, MA: Harvard University Press; 1963 [View Article]
     [Google Scholar]
  10. Pigliucci M. What, if anything, is an evolutionary novelty?. Philos of Sci 2008; 75:887–898 [View Article]
     [Google Scholar]
  11. Hochberg ME, Marquet PA, Boyd R, Wagner A. Innovation: an emerging focus from cells to societies. Phil Trans R Soc B 2017; 372:20160414 [View Article]
     [Google Scholar]
  12. Erwin DH. Novelty and innovation in the history of life. Curr Biol 2015; 25:R930–40 [View Article] [PubMed]
     [Google Scholar]
  13. Hohmann-Marriott MF, Blankenship RE. Evolution of photosynthesis. Annu Rev Plant Biol 2011; 62:515–548 [View Article] [PubMed]
     [Google Scholar]
  14. Knoll AH. The geological consequences of evolution. Geobiology 2003; 1:3–14 [View Article]
     [Google Scholar]
  15. Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK. The continuing puzzle of the great oxidation event. Curr Biol 2009; 19:R567–74 [View Article] [PubMed]
     [Google Scholar]
  16. Chen S-C, Sun G-X, Yan Y, Konstantinidis KT, Zhang S-Y et al. The great oxidation event expanded the genetic repertoire of arsenic metabolism and cycling. Proc Natl Acad Sci 2020; 117:10414–10421 [View Article]
     [Google Scholar]
  17. Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC. Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc Natl Acad Sci 2013; 110:1791–1796 [View Article] [PubMed]
     [Google Scholar]
  18. Sánchez-Baracaldo P, Cardona T. On the origin of oxygenic photosynthesis and Cyanobacteria. New Phytol 2020; 225:1440–1446 [View Article] [PubMed]
     [Google Scholar]
  19. Selifonova O, Valle F, Schellenberger V. Rapid evolution of novel traits in microorganisms. Appl Environ Microbiol 2001; 67:3645–3649 [View Article] [PubMed]
     [Google Scholar]
  20. Szappanos B, Fritzemeier J, Csörgő B, Lázár V, Lu X et al. Adaptive evolution of complex innovations through stepwise metabolic niche expansion. Nat Commun 2016; 7:11607 [View Article] [PubMed]
     [Google Scholar]
  21. Kirchberger PC, Schmidt ML, Ochman H. The ingenuity of bacterial genomes. Annu Rev Microbiol 2020; 74:815–834 [View Article] [PubMed]
     [Google Scholar]
  22. Brito IL. Examining horizontal gene transfer in microbial communities. Nat Rev Microbiol 2021; 19:442–453 [View Article] [PubMed]
     [Google Scholar]
  23. Karve S, Wagner A. Multiple novel traits without immediate benefits originate in bacteria evolving on single antibiotics. Mol Biol Evol 2022; 39:msab341 [View Article] [PubMed]
     [Google Scholar]
  24. Negoro S. Biodegradation of nylon oligomers. Appl Microbiol Biotechnol 2000; 54:461–466 [View Article] [PubMed]
     [Google Scholar]
  25. Smith NW, Shorten PR, Altermann E, Roy NC, McNabb WC. The classification and evolution of bacterial cross-feeding. Front Ecol Evol 2019; 7:153 [View Article]
     [Google Scholar]
  26. Seth EC, Taga ME. Nutrient cross-feeding in the microbial world. Front Microbiol 2014; 5:350 [View Article] [PubMed]
     [Google Scholar]
  27. Zengler K, Zaramela LS. The social network of microorganisms - how auxotrophies shape complex communities. Nat Rev Microbiol 2018; 16:383–390 [View Article] [PubMed]
     [Google Scholar]
  28. Pacheco AR, Segrè D. A multidimensional perspective on microbial interactions. FEMS Microbiol Lett 2019; 366:fnz125 [View Article] [PubMed]
     [Google Scholar]
  29. Kreft J-U, Griffin BM, González-Cabaleiro R. Evolutionary causes and consequences of metabolic division of labour: why anaerobes do and aerobes don’t. Curr Opin Biotechnol 2020; 62:80–87 [View Article] [PubMed]
     [Google Scholar]
  30. Mataigne V, Vannier N, Vandenkoornhuyse P, Hacquard S. Microbial systems ecology to understand cross-feeding in microbiomes. Front Microbiol 2021; 12:780469 [View Article] [PubMed]
     [Google Scholar]
  31. Henriques SF, Dhakan DB, Serra L, Francisco AP, Carvalho-Santos Z et al. Metabolic cross-feeding in imbalanced diets allows gut microbes to improve reproduction and alter host behaviour. Nat Commun 2020; 11:4236 [View Article] [PubMed]
     [Google Scholar]
  32. Clark RL, Connors BM, Stevenson DM, Hromada SE, Hamilton JJ et al. Design of synthetic human gut microbiome assembly and butyrate production. Nat Commun 2021; 12:3254 [View Article] [PubMed]
     [Google Scholar]
  33. Goyal A, Wang T, Dubinkina V, Maslov S. Ecology-guided prediction of cross-feeding interactions in the human gut microbiome. Nat Commun 2021; 12:1335 [View Article] [PubMed]
     [Google Scholar]
  34. San Roman M, Wagner A. Diversity begets diversity during community assembly until ecological limits impose a diversity ceiling. Mol Ecol 2021; 30:5874–5887 [View Article] [PubMed]
     [Google Scholar]
  35. Saa P, Urrutia A, Silva-Andrade C, Martín AJ, Garrido D. Modeling approaches for probing cross-feeding interactions in the human gut microbiome. Comput Struct Biotechnol J 2022; 20:79–89 [View Article] [PubMed]
     [Google Scholar]
  36. Rosenzweig RF, Sharp RR, Treves DS, Adams J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 1994; 137:903–917 [View Article] [PubMed]
     [Google Scholar]
  37. Treves DS, Manning S, Adams J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 1998; 15:789–797 [View Article] [PubMed]
     [Google Scholar]
  38. Behringer MG, Ho W-C, Meraz JC, Miller SF, Boyer GF et al. Complex ecotype dynamics evolve in response to fluctuating resources. mBio 2022; 13:e0346721 [View Article] [PubMed]
     [Google Scholar]
  39. Turner PE, Souza V, Lenski RE. Tests of ecological mechanisms promoting the stable coexistence of two bacterial genotypes. Ecology 1996; 77:2119–2129 [View Article]
     [Google Scholar]
  40. Großkopf T, Consuegra J, Gaffé J, Willison JC, Lenski RE et al. Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment. BMC Evol Biol 2016; 16:163 [View Article] [PubMed]
     [Google Scholar]
  41. Doebeli M. A model for the evolutionary dynamics of cross‐feeding polymorphisms in microorganisms. Popul Ecol 2002; 44:59–70 [View Article]
     [Google Scholar]
  42. Pfeiffer T, Bonhoeffer S. Evolution of cross-feeding in microbial populations. Am Nat 2004; 163:E126–35 [View Article] [PubMed]
     [Google Scholar]
  43. San Roman M, Wagner A. An enormous potential for niche construction through bacterial cross-feeding in a homogeneous environment. PLoS Comput Biol 2018; 14:e1006340 [View Article] [PubMed]
     [Google Scholar]
  44. Pacheco AR, Moel M, Segrè D. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. Nat Commun 2019; 10:103 [View Article] [PubMed]
     [Google Scholar]
  45. Lenski RE, Rose MR, Simpson SC, Tadler SC. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 1991; 138:1315–1341 [View Article]
     [Google Scholar]
  46. Lenski RE. Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations. ISME J 2017; 11:2181–2194 [View Article] [PubMed]
     [Google Scholar]
  47. Rozen DE, Lenski RE. Long‐term experimental evolution in Escherichia coli . VIII. Dynamics of a balanced polymorphism. Am Nat 2000; 155:24–35 [View Article]
     [Google Scholar]
  48. Le Gac M, Plucain J, Hindré T, Lenski RE, Schneider D. Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proc Natl Acad Sci 2012; 109:9487–9492 [View Article] [PubMed]
     [Google Scholar]
  49. Good BH, McDonald MJ, Barrick JE, Lenski RE, Desai MM. The dynamics of molecular evolution over 60,000 generations. Nature 2017; 551:45–50 [View Article]
     [Google Scholar]
  50. Maddamsetti R, Lenski RE, Barrick JE. Adaptation, clonal interference, and frequency-dependent interactions in a long-term evolution experiment with Escherichia coli. Genetics 2015; 200:619–631 [View Article] [PubMed]
     [Google Scholar]
  51. Ribeck N, Lenski RE. Modeling and quantifying frequency-dependent fitness in microbial populations with cross-feeding interactions. Evolution 2015; 69:1313–1320 [View Article] [PubMed]
     [Google Scholar]
  52. Blount ZD. A case study in evolutionary contingency. Stud Hist Philos of Sci C Stud Hist Philos Biol Biomed Sci 2016; 58:82–92
     [Google Scholar]
  53. Koser SA. Correlation of citrate-utilization by members of the colon-aerogenes group with other differential characteristics and with habitat. J Bacteriol 1924; 9:59–77 [View Article] [PubMed]
     [Google Scholar]
  54. Hall BG. Chromosomal mutation for citrate utilization by Escherichia coli K-12. J Bacteriol 1982; 151:269–273 [View Article] [PubMed]
     [Google Scholar]
  55. Blount ZD, Borland CZ, Lenski RE. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci 2008; 105:7899–7906 [View Article] [PubMed]
     [Google Scholar]
  56. Quandt EM, Gollihar J, Blount ZD, Ellington AD, Georgiou G et al. Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment. eLife 2015; 4:e09696 [View Article] [PubMed]
     [Google Scholar]
  57. Wiser MJ, Ribeck N, Lenski RE. Long-term dynamics of adaptation in asexual populations. Science 2013; 342:1364–1367 [View Article] [PubMed]
     [Google Scholar]
  58. Leon D, D’Alton S, Quandt EM, Barrick JE. Innovation in an E. coli evolution experiment is contingent on maintaining adaptive potential until competition subsides. PLoS Genet 2018; 14:e1007348 [View Article] [PubMed]
     [Google Scholar]
  59. Blount ZD, Barrick JE, Davidson CJ, Lenski RE. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 2012; 489:513–518 [View Article] [PubMed]
     [Google Scholar]
  60. Lutgens M, Gottschalk G. Why a co-substrate is required for anaerobic growth of Escherichia coli on citrate. Microbiology 1980; 119:63–70 [View Article]
     [Google Scholar]
  61. Bott M. Anaerobic citrate metabolism and its regulation in enterobacteria. Arch Microbiol 1997; 167:78–88 [PubMed]
     [Google Scholar]
  62. Pos KM, Dimroth P, Bott M. The Escherichia coli citrate carrier CitT: a member of a novel eubacterial transporter family related to the 2-oxoglutarate/malate translocator from spinach chloroplasts. J Bacteriol 1998; 180:4160–4165 [View Article] [PubMed]
     [Google Scholar]
  63. Leiby N, Marx CJ. Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biol 2014; 12:e1001789 [View Article] [PubMed]
     [Google Scholar]
  64. Barrick JE, Blount ZD, Lake DM, Dwenger JH, Chavarria-Palma JE et al. Daily transfers, archiving populations, and measuring fitness in the Long-Term Evolution Experiment with Escherichia coli. J Vis Exp 2023 [View Article]
     [Google Scholar]
  65. Blount ZD, Maddamsetti R, Grant NA, Ahmed ST, Jagdish T et al. Genomic and phenotypic evolution of Escherichia coli in a novel citrate-only resource environment. eLife 2020; 9:e55414 [View Article] [PubMed]
     [Google Scholar]
  66. Sambrook J, Russell D. Molecular Cloning: A Laboratory Manual New York, NY: Cold Spring Harbor Laboratory Press; 2001
     [Google Scholar]
  67. Levin BR, Stewart FM, Chao L. Resource-limited growth, competition, and predation: a model and experimental studies with bacteria and bacteriophage. Am Nat 1977; 111:3–24 [View Article]
     [Google Scholar]
  68. Meyer JR, Agrawal AA, Quick RT, Dobias DT, Schneider D et al. Parallel changes in host resistance to viral infection during 45,000 generations of relaxed selection. Evolution 2010; 64:3024–3034 [View Article] [PubMed]
     [Google Scholar]
  69. Pelosi L, Kühn L, Guetta D, Garin J, Geiselmann J et al. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 2006; 173:1851–1869 [View Article] [PubMed]
     [Google Scholar]
  70. Reddy CA, Beveridge TJ, Breznak JA, Marzluf GA, Schmidt TM et al. Methods for General and Molecular Microbiology Washington, DC, USA: American Society for Microbiology Press; 2007 [View Article]
     [Google Scholar]
  71. Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 2014; 1151:165–188 [View Article] [PubMed]
     [Google Scholar]
  72. Link AJ, Phillips D, Church GM. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 1997; 179:6228–6237 [View Article] [PubMed]
     [Google Scholar]
  73. Janausch IG, Garcia-Moreno I, Lehnen D, Zeuner Y, Unden G. Phosphorylation and DNA binding of the regulator DcuR of the fumarate-responsive two-component system DcuSR of Escherichia coli. Microbiology 2004; 150:877–883 [View Article] [PubMed]
     [Google Scholar]
  74. Jeong H, Barbe V, Lee CH, Vallenet D, Yu DS et al. Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J Mol Biol 2009; 394:644–652 [View Article] [PubMed]
     [Google Scholar]
  75. Yoon SH, Han M-J, Jeong H, Lee CH, Xia X-X et al. Comparative multi-omics systems analysis of Escherichia coli strains B and K-12. Genome Biol 2012; 13:1–13 [View Article] [PubMed]
     [Google Scholar]
  76. Quandt EM, Deatherage DE, Ellington AD, Georgiou G, Barrick JE. Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli. Proc Natl Acad Sci 2014; 111:2217–2222 [View Article] [PubMed]
     [Google Scholar]
  77. Nizam SA, Zhu J, Ho PY, Shimizu K. Effects of arcA and arcB genes knockout on the metabolism in Escherichia coli under aerobic condition. Biochem Eng J 2009; 44:240–250 [View Article]
     [Google Scholar]
  78. Moxon R, Bayliss C, Hood D. Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annual review of genetics 2006; 40:307–333 [View Article] [PubMed]
     [Google Scholar]
  79. Lenski RE. Revisiting the design of the long-term evolution experiment with Escherichia coli. J Mol Evol 2023; 91:241–253 [View Article] [PubMed]
     [Google Scholar]
  80. Lenski RE. Phenotypic and genomic evolution during a 20,000 generation experiment with the bacterium Eschericia coli. Plant Breed Rev 2004; 24:225–265
     [Google Scholar]
  81. Turner CB, Blount ZD, Lenski RE. Replaying evolution to test the cause of extinction of one ecotype in an experimentally evolved population. PLoS One 2015; 10:e0142050 [View Article] [PubMed]
     [Google Scholar]
  82. Davies SJ, Golby P, Omrani D, Broad SA, Harrington VL et al. Inactivation and regulation of the aerobic C(4)-dicarboxylate transport (dctA) gene of Escherichia coli. J Bacteriol 1999; 181:5624–5635 [View Article] [PubMed]
     [Google Scholar]
  83. Schubert C, Unden G. C4-dicarboxylates as growth substrates and signaling molecules for commensal and pathogenic enteric bacteria in mammalian intestine. J Bacteriol 2022; 204:e0054521 [View Article] [PubMed]
     [Google Scholar]
  84. Jacob F. Evolution and tinkering. Science 1977; 196:1161–1166 [View Article] [PubMed]
     [Google Scholar]
  85. Boorsma A, van der Rest ME, Lolkema JS, Konings WN. Secondary transporters for citrate and the Mg(2+)-citrate complex in Bacillus subtilis are homologous proteins. J Bacteriol 1996; 178:6216–6222 [View Article] [PubMed]
     [Google Scholar]
  86. Reynolds CH, Silver S. Citrate utilization by Escherichia coli: plasmid- and chromosome-encoded systems. J Bacteriol 1983; 156:1019–1024 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001390
Loading
Evolution of a cross-feeding interaction following a key innovation in a long-term evolution experiment with Escherichia coli
Microbiology 169, 001390 (2023); https://doi.org/10.1099/mic.0.001390
/content/journal/micro/10.1099/mic.0.001390
/content/journal/micro/10.1099/mic.0.001390
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error