Mechanism for microbial population collapse in a fluctuating resource environment

Molecular Systems Biology

Volumn 13, Issue 3, 2017, Pages

  Turkarslan, Serdar ^a   Raman, Arjun V ^a   Thompson, Anne W ^a   Arens, Christina E ^a   Gillespie, Mark A ^a   von Netzer, Frederick ^b   Hillesland, Kristina L ^c   Stolyar, Sergey ^a   López García de Lomana, Adrian ^a   Reiss, David J ^a   Gorman Lewis, Drew ^b   Zane, Grant M ^d   Ranish, Jeffrey A ^a   Wall, Judy D ^d   Stahl, David A ^b   Baliga, Nitin S ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON BOTHELL   (United States)

^d University of Missouri   (United States)

Author keywords

fluctuating resource environment; microbial population collapse; regulation; resilience; syntrophy

Indexed keywords

RNA; SULFATE; TRANSCRIPTOME;

ARTICLE; COCULTURE; CONTROLLED STUDY; DILUTION; FLOW CYTOMETRY; GENE CONTROL; GENE REGULATORY NETWORK; GENOTYPE; METHANOCOCCUS MARIPALUDIS; MICROBIAL COMMUNITY; MICROCALORIMETRY; MICROSCOPY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEOMICS; QUANTITATIVE ANALYSIS; RNA SEQUENCE; SIGNAL TRANSDUCTION; STEADY STATE; TRANSCRIPTOMICS; DESULFOVIBRIO VULGARIS; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METHANOCOCCUS; OXIDATION REDUCTION REACTION; PROCEDURES; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; SYSTEMS BIOLOGY;

DESULFOVIBRIO VULGARIS; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION PROFILING; METHANOCOCCUS; OXIDATION-REDUCTION; PHENOTYPE; PROTEOMICS; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS; SULFATES; SYSTEMS BIOLOGY;

EID: 85016245951     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20167058     Document Type: Article

References (67)

1. Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. (www.bioconductor.org).
2. Alon U (2007) An introduction to systems biology: design principles of biological circuits. London, UK: Chapman and Hall/CRC
3. Anders S, Pyl PT, Huber W (2015) HTSeq-A Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166–169
4. Andrews S (2010) FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
5. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MCH, Hood L, DiRuggiero J (2004) Systems level insights into the stress response to UV radiation in the Halophilic archaeon Halobacterium NRC-1. Genome Res 14: 1025–1035
6. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461: 1243–1247
7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57: 289–300
8. Blount ZD, Borland CZ, Lenski RE (2008) Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105: 7899–7906
9. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120
10. Bon M, McGowan SJ, Cook PR (2006) Many expressed genes in bacteria and yeast are transcribed only once per cell cycle. FASEB J 20: 1721–1723
11. Bonneau R, Reiss DJ, Shannon P, Facciotti M, Hood L, Baliga NS, Thorsson V (2006) The Inferelator: an algorithm for learning parsimonious regulatory networks from systems-biology data sets de novo. Genome Biol 7: R36
12. Bonneau R, Facciotti MT, Reiss DJ, Schmid AK, Pan M, Kaur A, Thorsson V, Shannon P, Johnson MH, Bare JC, Longabaugh W, Vuthoori M, Whitehead K, Madar A, Suzuki L, Mori T, Chang D-E, Diruggiero J, Johnson CH, Hood L et al (2007) A predictive model for transcriptional control of physiology in a free living cell. Cell 131: 1354–1365
13. Cai L, Friedman N, Xie XS (2006) Stochastic protein expression in individual cells at the single molecule level. Nature 440: 358–362
14. Chardin B, Dolla A, Chaspoul F, Fardeau M, Gallice P, Bruschi M (2003) Bioremediation of chromate: thermodynamic analysis of the effects of Cr(VI) on sulfate-reducing bacteria. Appl Microbiol Biotechnol 60: 352–360
15. Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99: 4044–4064
16. Chen A, Sanchez A, Dai L, Gore J (2014) Dynamics of a producer-freeloader ecosystem on the brink of collapse. Nat Commun 5: 3713
17. Choi PJ, Cai L, Frieda K, Xie XS (2008) A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 322: 442–446
18. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6: 80–92
19. Cooper VS, Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739
20. Cooper TF, Rozen DE, Lenski RE (2003) Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci USA 100: 1072–1077
21. Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367–1372
22. Cox J, Hein MY, Luber CA, Paron I (2014) Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell 13: 2513–2526
23. Deatherage DE, Barrick JE (2014) Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 1151: 165–188
24. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, Friedland GD, Huang KH, Keller K, Novichkov PS, Dubchak IL, Alm EJ, Arkin AP (2009) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38: D396–D400
25. Demirel B, Yenigün O (2002) Two-phase anaerobic digestion processes: a review. J Chem Technol Biotechnol 77: 743–755
26. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernytsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuler D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498
27. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15–21
28. Fels SR, Zane GM, Blake SM, Wall JD (2013) Rapid transposon liquid enrichment sequencing (TnLE-seq) for gene fitness evaluation in underdeveloped bacterial systems. Appl Environ Microbiol 79: 7510–7517
29. Fiegna F, Yu Y-TN, Kadam SV, Velicer GJ (2006) Evolution of an obligate social cheater to a superior cooperator. Nature 441: 310–314
30. Friedman N, Cai L, Xie X (2006) Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys Rev Lett 97: 168302
31. Fuhrman JA, Cram JA, Needham DM (2015) Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol 13: 133–146
32. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19: 207–233
33. Grenthe I, Ots H, Ginstrup O, Nielsen PH, Rasmussen SE, Sunde E, Sørensen NA (1970) A calorimetric determination of the enthalpy of ionization of water and the enthalpy of protonation of tham at 5, 20, 25, 35, and 50 degrees C. Acta Chem Scand 24: 1067–1080
34. Hillesland KL, Stahl DA (2010) Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci USA 107: 2124–2129
35. Hillesland KL, Lim S, Flowers JJ, Turkarslan S, Pinel N, Zane GM, Elliott N, Qin Y, Wu L, Baliga NS, Zhou J, Wall JD, Stahl DA (2014) Erosion of functional independence early in the evolution of a microbial mutualism. Proc Natl Acad Sci USA 111: 14822–14827
36. Hindré T, Knibbe C, Beslon G, Schneider D (2012) New insights into bacterial adaptation through in vivo and in silico experimental evolution. Nat Rev Microbiol 10: 352–365
37. Hottes AK, Freddolino PL, Khare A, Donnell ZN, Liu JC, Tavazoie S (2013) Bacterial adaptation through loss of function. PLoS Genet 9: e1003617
38. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57
39. Huh D, Paulsson J (2011) Non-genetic heterogeneity from stochastic partitioning at cell division. Nat Genet 43: 95–100
40. Johansson P, Wadsö I (1999) An isothermal microcalorimetric titration/perfusion vessel equipped with electrodes and spectrophotometer. Thermochim Acta 342: 19–29
41. Kashtan N, Alon U (2005) Spontaneous evolution of modularity and network motifs. Proc Natl Acad Sci USA 102: 13773–13778
42. Kato S, Kosaka T, Watanabe K (2009) Substrate-dependent transcriptomic shifts in Pelotomaculum thermopropionicum grown in syntrophic co-culture with Methanothermobacter thermautotrophicus. Microb Biotechnol 2: 575–584
43. Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22: 568–576
44. Koide T, Reiss DJ, Bare JC, Pang WL, Facciotti MT, Schmid AK, Pan M, Marzolf B, Van PT, Lo F-Y, Pratap A, Deutsch EW, Peterson A, Martin D, Baliga NS (2009) Prevalence of transcription promoters within archaeal operons and coding sequences. Mol Syst Biol 5: 285
45. Kosaka T, Kato S, Shimoyama T, Ishii S, Abe T, Watanabe K (2008) The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota. Genome Res 18: 442–448
46. Kurlandzka A, Rosenzweig RF, Adams J (1991) Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. Mol Biol Evol 8: 261–281
47. Lee M-C, Chou H-H, Marx CJ (2009) Asymmetric, bimodal trade-offs during adaptation of Methylobacterium to distinct growth substrates. Evolution 63: 2816–2830
48. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760
49. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550
50. Michalski A, Damoc E, Lange O, Denisov E, Nolting D, Muller M, Viner R, Schwartz J, Remes P, Belford M, Dunyach J-J, Cox J, Horning S, Mann M, Makarov A (2012) Ultra high resolution linear ion trap orbitrap mass spectrometer (Orbitrap Elite) facilitates top down LC MS/MS and versatile peptide fragmentation modes. Mol Cell Proteomics 11: O111.013698
51. Nagarajan H, Embree M, Rotaru A-E, Shrestha PM, Feist AM, Palsson BØ, Lovley DR, Zengler K (2013) Characterization and modelling of interspecies electron transfer mechanisms and microbial community dynamics of a syntrophic association. Nat Commun 4: 2809
52. Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY, Sutormin RA, Kazanov MD, Riehl W, Arkin AP, Dubchak I, Rodionov DA (2013) RegPrecise 3.0–a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genom 14: 745
53. Parter M, Kashtan N, Alon U (2007) Environmental variability and modularity of bacterial metabolic networks. BMC Evol Biol 7: 169
54. Plugge CM, Scholten JCM, Culley DE, Nie L, Brockman FJ, Zhang W (2010) Global transcriptomics analysis of the Desulfovibrio vulgaris change from syntrophic growth with Methanosarcina barkeri to sulfidogenic metabolism. Microbiology 156: 2746–2756
55. Reiss DJ, Baliga NS, Bonneau R (2006) Integrated biclustering of heterogeneous genome-wide datasets for the inference of global regulatory networks. BMC Bioinformatics 7: 280
56. Shimoyama T, Kato S, Ishii S, Watanabe K (2009) Flagellum mediates symbiosis. Science 323: 1574
57. Song H-S, Renslow RS, Fredrickson JK, Lindemann SR (2015) Integrating ecological and engineering concepts of resilience in microbial communities. Front Microbiol 6: 1298
58. Ståhlberg A, Rusnakova V, Forootan A, Anderova M, Kubista M (2013) RT-qPCR work-flow for single-cell data analysis. Methods 59: 80–88
59. von Stockar U, Liu J-S (1999) Does microbial life always feed on negative entropy? Thermodynamic analysis of microbial growth. Biochim Biophys Acta - Bioenerg 1412: 191–211
60. von Stockar U, Maskow T, Liu J, Marison IW, Patiño R (2006) Thermodynamics of microbial growth and metabolism: an analysis of the current situation. J Biotechnol 121: 517–533
61. Stolyar S, Van Dien S, Hillesland KL, Pinel N, Lie TJ, Leigh JA, Stahl DA (2007) Metabolic modeling of a mutualistic microbial community. Mol Syst Biol 3: 92
62. Thompson AW, Crow MJ, Wadey B, Arens C, Turkarslan S, Stolyar S, Elliott N, Petersen TW, van den Engh G, Stahl DA, Baliga NS (2015) A method to analyze, sort, and retain viability of obligate anaerobic microorganisms from complex microbial communities. J Microbiol Methods 117: 74–77
63. Turkarslan S, Reiss DJ, Gibbins G, Su WL, Pan M, Bare JC, Plaisier CL, Baliga NS (2011) Niche adaptation by expansion and reprogramming of general transcription factors. Mol Syst Biol 7: 554
64. Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods 13: 731–740
65. Wadso I, Goldberg RN (2001) Standards in isothermal microcalorimetry (IUPAC Technical Report). Pure Appl Chem 73: 1625–1639
66. Walker CB, He Z, Yang ZK, Ringbauer JA, He Q, Zhou J, Voordouw G, Wall JD, Arkin AP, Hazen TC, Stolyar S, Stahl DA (2009) The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J Bacteriol 191: 5793–5801
67. Yang L, Jelsbak L, Marvig RL, Damkiær S, Workman CT, Rau MH, Hansen SK, Folkesson A, Johansen HK, Ciofu O, Høiby N, Sommer MOA, Molin S (2011) Evolutionary dynamics of bacteria in a human host environment. Proc Natl Acad Sci USA 108: 7481–7486