Long-term adaptive evolution of Shewanella oneidensis MR-1 for establishment of high concentration Cr(VI) tolerance

Abstract

• Shewanella oneidensis MR-1 was acclimated to grow with Cr(VI) of 190 mg/L.

• Whole genomes from 7 populations at different acclimation stages were sequenced.

• Gene mutations mainly related to efflux pumps and transporters.

• An adaptation mechanism of MR-1 to high concentration of Cr(VI) was proposed.

Acclimation is the main method to enhance the productivity of microorganisms in environmental biotechnology, but it remains uncertain how microorganisms acquire resistance to high concentrations of pollutants during long-term acclimation. Shewanella oneidensis MR-1 was acclimated for 120 days with increasing hexavalent chromium (Cr(VI)) concentrations from 10 to 190 mg/L. The bacterium was able to survive from the highly toxic Cr(VI) environment due to its enhanced capability to reduce Cr(VI) and the increased cell membrane surface. We sequenced 19 complete genomes from 7 populations of MR-1, including the ancestral strain, the evolved strains in Cr(VI) environment on days 40, 80 and 120 and their corresponding controls. A total of 27, 49 and 90 single nucleotide polymorphisms were found in the Cr(VI)-evolved populations on days 40, 80 and 120, respectively. Nonsynonymous substitutions were clustered according to gene functions, and the gene mutations related to integral components of the membrane, including efflux pumps and transporters, were the key determinants of chromate resistance. In addition, MR-1 strengthened the detoxification of Cr(VI) through gene variations involved in adenosine triphosphate binding, electron carrier activity, signal transduction and DNA repair. Our results provide an in-depth analysis of how Cr(VI) resistance of S. oneidensis MR-1 is improved by acclimation, as well as a genetic understanding of the impact of long-term exposure of microorganisms to pollution.

Graphical abstract

Keywords

Environmental biotechnology / Acclimation / Chromate resistance / Efflux pumps / Detoxification

References

[1] Aguilera S, Aguilar M E, Chávez M P, López-Meza J E, Pedraza-Reyes M, Campos-García J, Cervantes C (2004). Essential residues in the chromate transporter ChrA of Pseudomonas aeruginosa. FEMS Microbiology Letters, 232(1): 107–112

[2] Barrick J E, Yu D S, Yoon S H, Jeong H, Oh T K, Schneider D, Lenski R E, Kim J F (2009). Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature, 461(7268): 1243–1247

[3] Bhatter P, Chatterjee A, D’souza D, Tolani M, Mistry N (2012). Estimating fitness by competition assays between drug susceptible and resistant Mycobacterium tuberculosis of predominant lineages in Mumbai, India. PLoS One, 7(3): e33507

[4] Blount Z D, Barrick J E, Davidson C J, Lenski R E (2012). Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature, 489(7417): 513–518

[5] Brockhurst M A, Colegrave N, Rozen D E (2011). Next-generation sequencing as a tool to study microbial evolution. Molecular Ecology, 20(5): 972–980

[6] Brown S D, Thompson M R, Verberkmoes N C, Chourey K, Shah M, Zhou J, Hettich R L, Thompson D K (2006). Molecular dynamics of the Shewanella oneidensis response to chromate stress. Molecular & Cellular Proteomics, 5(6): 1054–1071

[7] Carlson H K, Price M N, Callaghan M, Aaring A, Chakraborty R, Liu H, Kuehl J V, Arkin A P, Deutschbauer A M (2019). The selective pressures on the microbial community in a metal-contaminated aquifer. The ISME Journal, 13(4): 937–949

[8] Cervantes C, Silver S (1992). Plasmid chromate resistance and chromate reduction. Plasmid, 27(1): 65–71

[9] Cheung K H, Gu J D (2007). Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: A review. International Biodeterioration & Biodegradation, 59(1): 8–15

[10] Choi O, Hu Z (2008). Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environmental Science & Technology, 42(12): 4583–4588

[11] Chourey K, Thompson M R, Morrell-Falvey J, Verberkmoes N C, Brown S D, Shah M, Zhou J, Doktycz M, Hettich R L, Thompson D K (2006). Global molecular and morphological effects of 24-hour chromium(VI) exposure on Shewanella oneidensis MR-1. Applied and Environmental Microbiology, 72(9): 6331–6344

[12] Cingolani P, Platts A, Wang L, Coon M, Nguyen T, Wang L, Land S J, Lu X, Ruden D M (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly, 6(2): 80–92

[13] Conrad T M, Lewis N E, Palsson B Ø (2011). Microbial laboratory evolution in the era of genome-scale science. Molecular Systems Biology, 7(1): 509

[14] Dettman J R, Rodrigue N, Melnyk A H, Wong A, Bailey S F, Kassen R (2012). Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Molecular Ecology, 21(9): 2058–2077

[15] Deutscher J, Francke C, Postma P W (2006). How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiology and Molecular Biology Reviews, 70(4): 939–1031

[16] Gang H, Xiao C, Xiao Y, Yan W, Bai R, Ding R, Yang Z, Zhao F (2019). Proteomic analysis of the reduction and resistance mechanisms of Shewanella oneidensis MR-1 under long-term hexavalent chromium stress. Environment International, 127: 94–102

[17] Gao H, Yang Z K, Wu L, Thompson D K, Zhou J (2006). Global transcriptome analysis of the cold shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold shock proteins. Journal of Bacteriology, 188(12): 4560–4569

[18] Gerrish P J, Lenski R E (1998). The fate of competing beneficial mutations in an asexual population. Genetica, 102/103(1-6): 127–144

[19] Groh J L, Luo Q, Ballard J D, Krumholz L R (2007). Genes that enhance the ecological fitness of Shewanella oneidensis MR-1 in sediments reveal the value of antibiotic resistance. Applied and Environmental Microbiology, 73(2): 492–498

[20] He Q, Xu P, Zhang C, Zeng G, Liu Z, Wang D, Tang W, Dong H, Tan X, Duan A (2019). Influence of surfactants on anaerobic digestion of waste activated sludge: acid and methane production and pollution removal. Critical Reviews in Biotechnology, 39(5): 746–757

[21] Heidelberg J F, Paulsen I T, Nelson K E, Gaidos E J, Nelson W C, Read T D, Eisen J A, Seshadri R, Ward N, Methe B, Clayton R A, Meyer T, Tsapin A, Scott J, Beanan M, Brinkac L, Daugherty S, DeBoy R T, Dodson R J, Durkin A S, Haft D H, Kolonay J F, Madupu R, Peterson J D, Umayam L A, White O, Wolf A M, Vamathevan J, Weidman J, Impraim M, Lee K, Berry K, Lee C, Mueller J, Khouri H, Gill J, Utterback T R, McDonald L A, Feldblyum T V, Smith H O, Venter J C, Nealson K H, Fraser C M (2002). Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnology, 20(11): 1118–1123

[22] Holmes D E, O’Neil R A, Chavan M A, N’Guessan L A, Vrionis H A, Perpetua L A, Larrahondo M J, DiDonato R, Liu A, Lovley D R (2009). Transcriptome of Geobacter uraniireducens growing in uranium-contaminated subsurface sediments. The ISME Journal, 3(2): 216–230

[23] Hou X, Huang L, Zhou P, Xue H, Li N (2018). Response of indigenous Cd-tolerant electrochemically active bacteria in MECs toward exotic Cr (VI) based on the sensing of fluorescence probes. Frontiers of Environmental Science & Engineering, 12(4): 7

[24] Hu H, Jin Q, Kavan P (2014). A study of heavy metal pollution in China: Current status, pollution-control policies and countermeasures. Sustainability, 6(9): 5820–5838

[25] Huang W, Sherman B T, Lempicki R A (2009a). Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research, 37(1): 1–13

[26] Huang W, Sherman B T, Lempicki R A (2009b). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 4(1): 44–57

[27] Korotkov K V, Sandkvist M, Hol W G J (2012). The type II secretion system: Biogenesis, molecular architecture and mechanism. Nature Reviews. Microbiology, 10(5): 336–351

[28] Kouzuma A, Oba H, Tajima N, Hashimoto K, Watanabe K (2014). Electrochemical selection and characterization of a high current-generating Shewanella oneidensis mutant with altered cell-surface morphology and biofilm-related gene expression. BMC Microbiology, 14(1): 190

[29] Lenski R E, Rose M R, Simpson S C, Tadler S C (1991). Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. American Naturalist, 138(6): 1315–1341

[30] Li H, Durbin R (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England), 25(14): 1754–1760

[31] Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, and the 1000 Genome Project Data Processing Subgroup (2009). The sequence alignment/map format and SAMtools. Bioinformatics (Oxford, England), 25(16): 2078–2079

[32] Li Z, Ma Z, van der Kuijp T J, Yuan Z, Huang L (2014). A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. The Science of the Total Environment, 468–469: 843–853

[33] Liang Q, Liu X, Zeng G, Liu Z, Tang L, Shao B, Zeng Z, Zhang W, Liu Y, Cheng M, Tang W, Gong S (2019). Surfactant-assisted synthesis of photocatalysts: Mechanism, synthesis, recent advances and environmental application. Chemical Engineering Journal, 372: 429–451

[34] Liu Z, Liu Y, Zeng G, Shao B, Chen M, Li Z, Jiang Y, Liu Y, Zhang Y, Zhong H (2018). Application of molecular docking for the degradation of organic pollutants in the environmental remediation: A review. Chemosphere, 203: 139–150

[35] Lytle C M, Lytle F W, Yang N, Qian J H, Hansen D, Zayed A, Terry N (1998). Reduction of Cr (VI) to Cr (III) by wetland plants: Potential for in situ heavy metal detoxification. Environmental Science & Technology, 32(20): 3087–3093

[36] McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M A (2010). The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9): 1297–1303

[37] Mikolay A, Nies D H (2009). The ABC-transporter AtmA is involved in nickel and cobalt resistance of Cupriavidus metallidurans strain CH34. Antonie van Leeuwenhoek, 96(2): 183–191

[38] Nishioka H (1975). Mutagenic activities of metal compounds in bacteria. Mutation Research, 31(3): 185–189

[39] Orellana R, Hixson K K, Murphy S, Mester T, Sharma M L, Lipton M S, Lovley D R (2014). Proteome of Geobacter sulfurreducens in the presence of U(VI). Microbiology, 160(12): 2607–2617

[40] Park C H, Keyhan M, Wielinga B, Fendorf S, Matin A (2000). Purification to homogeneity and characterization of a novel Pseudomonas putida chromate reductase. Applied and Environmental Microbiology, 66(5): 1788–1795

[41] Petrilli F L, De Flora S (1977). Toxicity and mutagenicity of hexavalent chromium on Salmonella typhimurium. Applied and Environmental Microbiology, 33(4): 805–809

[42] Puentes-Téllez P E, Hansen M A, Sørensen S J, van Elsas J D (2013). Adaptation and heterogeneity of Escherichia coli MC1000 growing in complex environments. Applied and Environmental Microbiology, 79(3): 1008–1017

[43] Qiu X, Sundin G W, Wu L, Zhou J, Tiedje J M (2005). Comparative analysis of differentially expressed genes in Shewanella oneidensis MR-1 following exposure to UVC, UVB, and UVA radiation. Journal of Bacteriology, 187(10): 3556–3564

[44] Rittmann B E, Hausner M, Löffler F, Love N G, Muyzer G, Okabe S, Oerther D B, Peccia J, Raskin L, Wagner M (2006). A vista for microbial ecology and environmental biotechnology. Environmental Science & Technology, 40(4): 1096–1103

[45] Torres-García W, Brown S D, Johnson R H, Zhang W, Runger G C, Meldrum D R (2011). Integrative analysis of transcriptomic and proteomic data of Shewanella oneidensis: Missing value imputation using temporal datasets. Molecular BioSystems, 7(4): 1093–1104

[46] Venkateswaran K, Moser D P, Dollhopf M E, Lies D P, Saffarini D A, MacGregor B J, Ringelberg D B, White D C, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson K H (1999). Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. International Journal of Systematic Bacteriology, 49(2): 705–724

[47] Viamajala S, Peyton B M, Apel W A, Petersen J N (2002). Chromate/nitrite interactions in Shewanella oneidensis MR-1: Evidence for multiple hexavalent chromium [Cr(VI)] reduction mechanisms dependent on physiological growth conditions. Biotechnology and Bioengineering, 78(7): 770–778

[48] Wang C, Chen J, Hu W J, Liu J Y, Zheng H L, Zhao F (2014). Comparative proteomics reveal the impact of OmcA/MtrC deletion on Shewanella oneidensis MR-1 in response to hexavalent chromium exposure. Applied Microbiology and Biotechnology, 98(23): 9735–9747

[49] Yang Z, Bielawski J P (2000). Statistical methods for detecting molecular adaptation. Trends in Ecology & Evolution, 15(12): 496–503

[50] Zeng Z, Liu X, Yao J, Guo Y, Li B, Li Y, Jiao N, Wang X (2016). Cold adaptation regulated by cryptic prophage excision in Shewanella oneidensis. The ISME Journal, 10(12): 2787–2800

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