Substrate cross-feeding affects the speed and trajectory of molecular evolution within a synthetic microbial assemblage
Tóm tắt
Substrate cross-feeding occurs when one organism partially consumes a primary substrate into one or more metabolites while other organisms then consume the metabolites. While pervasive within microbial communities, our knowledge about the effects of substrate cross-feeding on microbial evolution remains limited. To address this knowledge gap, we experimentally evolved isogenic nitrite (NO2−) cross-feeding microbial strains together for 700 generations, identified genetic changes that were acquired over the evolution experiment, and compared the results with an isogenic completely denitrifying strain that was evolved alone for 700 generations. We further investigated how the magnitude of interdependence between the nitrite cross-feeding strains affects the main outcomes. Our main objective was to quantify how substrate cross-feeding and the magnitude of interdependence affect the speed and trajectory of molecular evolution. We found that each nitrite (NO2−) cross-feeding strain acquired fewer genetic changes than did the completely denitrifying strain. In contrast, pairs of nitrite cross-feeding strains together acquired more genetic changes than did the completely denitrifying strain. Moreover, nitrite cross-feeding promoted population diversification, as pairs of nitrite cross-feeding strains acquired a more varied set of genetic changes than did the completely denitrifying strain. These outcomes likely occurred because nitrite cross-feeding enabled the co-existence of two distinct microbial strains, thus increasing the amount of genetic variation for selection to act upon. Finally, the nitrite cross-feeding strains acquired different types of genetic changes than did the completely denitrifying strain, indicating that nitrite cross-feeding modulates the trajectory of molecular evolution. Our results demonstrate that substrate cross-feeding can affect both the speed and trajectory of molecular evolution within microbial populations. Substrate cross-feeding can therefore have potentially important effects on the life histories of microorganisms.
Tài liệu tham khảo
Johnson DR, Goldschmidt F, Lilja EE, Ackermann M. Metabolic specialization and the assembly of microbial communities. ISME J. 2012;6:1985–91.
Seth EC, Taga ME. Nutrient cross-feeding in the microbial world. Front Microbiol. 2014;5:350.
Morris JJ, Lenski RE, Zinser ER. The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio. 2012;3:e00036–12.
Abreu N, Taga M. Decoding molecular interactions in microbial communities. FEMS Microbiol Rev. 2016;40:648–63.
Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016;7:13219.
Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev. 1997;61:262–80.
Martienssen M, Schöps R. Population dynamics of denitrifying bacteria in a model biocommunity. Water Res. 1999;33:639–46.
Pelz O, Tesar M, Wittich RM, Moore ER, Timmis KN, Abraham WR. Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol. 1999;1:167–74.
Christensen BB, Haagensen JAJ, Heydorn A, Molin S. Metabolic commensalism and competition in a two-species microbial consortium. Appl Environ Microbiol. 2002;68:2495–502.
McInerney MJ, Sieber JR, Gunsalus RP. Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol. 2009;20:623–32.
De Vuyst L, Leroy F. Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol. 2011;149:73–80.
Lilja EE, Johnson DR. Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates. ISME J. 2016;10:1568–78.
Hillesland KL, Stahl DA. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci U S A. 2010;107:2124–9.
Hillesland KL, Lim S, Flowers JJ, Turkarslan S, Pinel N, Zane GM, et al. Erosion of functional independence early in the evolution of a microbial mutualism. Proc Natl Acad Sci U S A. 2014;111:14822–7.
Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ, Thomson NR, et al. Antagonistic coevolution accelerates molecular evolution. Nature. 2010;464:275–8.
Pande S, Kaftan F, Lang S, Svatoš A, Germerodt S, Cost C. Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments. ISME J. 2016;10:1413–23.
Marchal M, Goldschmidt F, Derksen-Müller SN, Panke S, Ackermann M, Johnson DR. A passive mutualistic interaction promotes the evolution of spatial structure within microbial populations. BMC Evol Biol. 2017;17:106.
Arjan JA, Visser M, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE. Diminishing returns from mutation supply rate in asexual populations. Science. 1999;283:404–6.
Lanfear R, Kokko H, Eyre-Walker A. Population size and the rate of evolution. Trends Ecol Evol. 2014;29:33–41.
Lilja EE, Johnson DR. Metabolite toxicity determines the pace of molecular evolution within microbial populations. BMC Evol Biol. 2017;17:52.
Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, et al. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci U S A. 2008;105:7564–9.
Yan Y, Ping S, Peng J, Han Y, Li L, Yang J, et al. Global transcriptional analysis of nitrogen fixation and ammonium repression in root-associated Pseudomonas stutzeri A1501. BMC Genomics. 2010;11:11.
Zumft WG. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev. 1997;61:533–616.
Lalucat J, Bennasar A, Bosch R, García-Valdés E, Palleroni NJ. Biology of Pseudomonas stutzeri. Microbiol Mol Biol Rev. 2006;70:510–47.
Goldschmidt F, Regoes RR, Johnson DR. Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations. ISME J. 2017;11:2112–23.
Goldschmidt F, Regoes RR, Johnson DR. Metabolite toxicity slows local diversity loss during expansion of a microbial cross-feeding community. ISME J. 2018;12:136–44.
Zumft WG. The biological role of nitric oxide in bacteria. Arch Microbiol. 1993;160:253–64.
Almeida JS, Julio SM, Reis MAM, Carrondo MJT. Nitrite inhibition of denitrification by Pseudomonas fluorescens. Biotechnol Bioeng. 1995;46:194–201.
Sijbesma WFH, Almeida JS, Reis MAM, Santos H. Uncoupling effect of nitrite during denitrification by Pseudomonas fluorescens: an in vivo 31P-NMR study. Biotechnol Bioeng. 1996;52:176–82.
Baumann B, van der Meer JR, Snozzi M, Zehnder AJB. Inhibition of denitrification activity but not of mRNA induction in Paracoccus dentrificans by nitrite at a suboptimal pH. Antonie Van Leeuwenhoek. 1997;72:183–9.
Zhou Y, Oehmen A, Lim M, Vadivelu V, Ng WJ. The role of nitrite and free nitrous acid (FNA) in wastewater treatment plants. Water Res. 2011;45:4672–82.
Goosen N, Moolenaar GF. Role of ATP hydrolysis by UvrA and UvrB during nucleotide excision repair. Res Microbiol. 2001;152:401–9.
Jaciuk M, Nowak E, Skowronek K, Tańska A, Nowotny M. Structure of UvrA nucleotide excision repair protein in complex with modified DNA. Nat Struct Mol Biol. 2011;18:191–7.
Winsor GL, Lam DKW, Fleming L, Lo R, Whiteside MD, Yu NY, et al. Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 2011;39:596–600.
Härtig E, Schiek U, Vollack KU, Zumft WG. Nitrate and nitrite control of respiratory nitrate reduction in denitrifying Pseudomonas stutzeri by a two-component regulatory system homologous to NarXL of Escherichia coli. J Bacteriol. 1999;181:3658–65.
Couce A, Tenaillon OA. The rule of declining adaptability in microbial evolution experiments. Front Genet. 2015;6:99.
Wong A, Seguin K. Effects of genotype on rates of substitution during experimental evolution. Evol. 2015;69:1772–85.
Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL. Conditionally replicative and conjugative plasmids carrying lacY alpha for cloning, mutagenesis, and allele replacement. Plasmid. 1996;35:1–13.
Minoia M, Gaillard M, Reinhard F, Stojanov M, Sentchilo V, van der Meer JR. Stochasticity and bistability in horizontal transfer control of a genomic island in Pseudomonas. Proc Natl Acad Sci U S A. 2008;105:20792–7.
Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, et al. A Tn7-based broad-range bacterial cloning and expression system. Nat Methods. 2005;2:443–8.
Coyle CL, Zumft WG, Kroneck PM, Korner H, Jakob W. Nitrous oxide reductase from denitrifying Pseudomonas perfectomarina. Purification and properties of a novel multicopper enzyme. Eur J Biochem. 1985;153:459–67.
Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27:863–4.
Deatherage DE, Barrick JE. Identification of mutations in laboratory evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol. 2014;1151:165–8.