Abstract
The Salar de Huasco is an evaporitic basin located in the Chilean Altiplano, which presents extreme environmental conditions for life, i.e. high altitude (3800 m.a.s.l.), negative water balance, a wide salinity range, high daily temperature changes and the occurrence of the highest registered solar radiation on the planet (> 1200 W m−2). This ecosystem is considered as a natural laboratory to understand different adaptations of microorganisms to extreme conditions. Rhodobacter, an anoxygenic aerobic phototrophic bacterial genus, represents one of the most abundant groups reported based on taxonomic diversity surveys in this ecosystem. The bacterial mat isolate Rhodobacter sp. strain Rb3 was used to study adaptation mechanisms to stress-inducing factors potentially explaining its success in a polyextreme ecosystem. We found that the Rhodobacter sp. Rb3 genome was characterized by a high abundance of genes involved in stress tolerance and adaptation strategies, among which DNA repair and oxidative stress were the most conspicuous. Moreover, many other molecular mechanisms associated with oxidative stress, photooxidation and antioxidants; DNA repair and protection; motility, chemotaxis and biofilm synthesis; osmotic stress, metal, metalloid and toxic anions resistance; antimicrobial resistance and multidrug pumps; sporulation; cold shock and heat shock stress; mobile genetic elements and toxin–antitoxin system were detected and identified as potential survival mechanism features in Rhodobacter sp. Rb3. In total, these results reveal a wide set of strategies used by the isolate to adapt and thrive under environmental stress conditions as a model of polyextreme environmental resistome.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilar P, Acosta E, Dorador C, Sommaruga R (2016) Large differences in bacterial community composition among three nearby extreme waterbodies of the high Andean plateau. Front Microbiol 7:976. https://doi.org/10.3389/fmicb.2016.00976
Albarracín VH, Pathak GP, Douki T, Cadet J, Borsarelli CD, Gärtner W, Farías ME (2012) Extremophilic Acinetobacter strains from high-altitude lakes in Argentinean Puna: remarkable UV-B resistance and efficient DNA damage repair. Orig Life Evol Biosph 42:201–221. https://doi.org/10.1007/s11084-012-9276-3
Albarracín VH, Simon J, Pathak GP, Valle L, Douki T, Cadet J, Borsarelli CD, Farías ME, Gärtner W (2014) First characterisation of a CPD-class I photolyase from a UV-resistant extremophile isolated from High-Altitude Andean Lakes. Photochem Photobiol Sci 13:739–750. https://doi.org/10.1039/C3PP50399B
Albarracín VH, Kurth D, Ordoñez OF et al (2015) High-up: a remote reservoir of microbial extremophiles in central Andean Wetlands. Front Microbiol 6:1404. https://doi.org/10.3389/fmicb.2015.01404
Altendorf K, Booth IR, Gralla JD, Greie JC, Rosenthal AZ, Wood JM (2009) Osmotic stress. In: Curtiss R III et al (eds) EcoSal Escherichia coli and Salmonella:cellular and molecular biology. ASM Press, Washington, DC. https://doi.org/10.1128/ecosalplus.5.4.5
Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158. https://doi.org/10.3389/fmicb.2011.00158
Arnoux B, Ducruix F, Reiss-Husson F, Lutz M, Norris J, Schiffer M, Chang CH (1989) Structure of spheroidene in the photosynthetic reaction center from Y Rhodobacter sphaeroides. FEBS Lett 258(1):47–50
Augusto-Pinto L, Regis da Silva CG, de Oliveira Lopes D, Machado-Silva A, Machado CR (2003) Escherichia coli as a model system to study DNA repair genes of eukaryotic organisms. Genet Mol Res 2(1):77–91
Bakhlanova IV, Dudkina AV, Baitin DM (2013) Enzymatic control of homologous recombination in Escherichia coli cells and hyper-recombination. Mol Biol 47(2):205–217. https://doi.org/10.7868/S0026898413020031
Bebout BM, Garcia-Pichel F (1995) UV B-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61(12):4215–4222
Bentchikou E, Servant P, Coste G, Sommer S (2010) A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet 6(1):e1000774. https://doi.org/10.1371/journal.pgen.1000774
Berg HC (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72(1):19–54. https://doi.org/10.1146/annurev.biochem.72.121801.161737
Bergholz PW, Bakermans C, Tiedje JM (2009) Psychrobacter arcticus 273-4 uses resource efficiency and molecular motion adaptations for subzero temperature growth. J Bacteriol 191(7):2340–2352. https://doi.org/10.1128/JB.01377-08
Berglund B (2015) Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics. Infect Ecol Epidemiol 5:28564. https://doi.org/10.3402/iee.v5.28564
Berndt C, Lillig CH, Holmgren A (2008) Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 1783(4):641–650. https://doi.org/10.1016/j.bbamcr.2008.02.003
Blanco P, Hernando-Amado S, Reales-Calderon JA, Corona F, Lira F, Alcalde-Rico M et al (2016) Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants. Microorganisms 4(1):14. https://doi.org/10.3390/microorganisms4010014
Boscari A, Mandon K, Dupont L, Poggi MC, Le Rudulier D (2002) BetS is a major glycine betaine/proline betaine transporter required for early osmotic adjustment in Sinorhizobium meliloti. J Bacteriol 184(10):2654–2663. https://doi.org/10.1128/JB.184.10.2654-2663.2002
Bugay AN, Krasavin EA, Parkhomenko AY, Vasilyeva MA (2015) Modeling nucleotide excision repair and its impact on UV-induced mutagenesis during SOS-response in bacterial cells. J Theor Biol 364:7–20. https://doi.org/10.1016/j.jtbi.2014.08.041
Cabiscol E, Tamarit J, Ros J (2000) Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3(1):3–8
Cadet J, Wagner JR (2013) DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harb Perspect Biol 5(2):a012559. https://doi.org/10.1101/cshperspect.a012559
Casanueva A, Tuffin M, Cary C, Cowan DA (2010) Molecular adaptations to psychrophily: the impact of “omic” technologies. Trends Microbiol 18(8):374–381. https://doi.org/10.1016/j.tim.2010.05.002
Castro-Severyn J, Remonsellez F, Valenzuela SL, Salinas C, Fortt J, Aguilar P et al (2017) Comparative genomics analysis of a new Exiguobacterium strain from Salar de Huasco reveals a repertoire of stress-related genes and arsenic resistance. Front Microbiol 8:456. https://doi.org/10.3389/fmicb.2017.00456
Chandrangsu P, Rensing C, Helmann JD (2017) Metal homeostasis and resistance in bacteria. Nat Rev Microbiol 15:338–350. https://doi.org/10.1038/nrmicro.2017.15
Chen L, Spiliotis ET, Roberts MF (1998) Biosynthesis of Di-myo-Inositol-1,1′-Phosphate, a novel osmolyte in hyperthermophilic archaea. J Bacteriol 180(15):3785–3792
Chen LZ, Wang GH, Hong S, Liu A, Li C, Liu YD (2009) UV-B-induced oxidative damage and protective role of exopolysaccharides in desert cyanobacterium Microcoleus vaginatus. J Integr plant Biol 51(2):194–200. https://doi.org/10.1111/j.1744-7909.2008.00784.x
Christensen-Dalsgaard M, Gerdes K (2006) Two higBA loci in the Vibrio cholerae superintegron encode mRNA cleaving enzymes and can stabilize plasmids. Mol Microbiol 62(2):397–411. https://doi.org/10.1111/j.1365-2958.2006.05385.x
Coussens NP, Daines DA (2016) Wake me when it’s over—bacterial toxin–antitoxin proteins and induced dormancy. Exp Biol Med 241:1332–1342. https://doi.org/10.1177/1535370216651938
de Bruijn FJ (2016) Stress and environmental regulation of gene expression and adaptation in bacteria, 1st edn. Wiley, New Jersey. https://doi.org/10.1002/9781119004813
Dib J, Motok J, Zenoff VF, Ordoñez O, Farías ME (2008) Occurrence of resistance to antibiotics, UV-B, and arsenic in bacteria isolated from extreme environments in high-altitude (above 4400 m) Andean wetlands. Curr Microbiol 56(5):510–517. https://doi.org/10.1007/s00284-008-9103-2
Dorador C, Vila I, Remonsellez F, Imhoff JF, Witzel KP (2010) Unique clusters of Archaea in Salar de Huasco, an athalassohaline evaporitic basin of the Chilean Altiplano. FEMS Microbiol Ecol 73(2):291–302. https://doi.org/10.1111/j.1574-6941.2010.00891.x
Dorador C, Vila I, Witzel KP, Imhoff JF (2013) Bacterial and archaeal diversity in high altitude wetlands of the Chilean Altiplano. Fund Appl Limnol 182(2):135–159. https://doi.org/10.1127/1863-9135/2013/0393
Fiebig A, Castro Rojas CM, Siegal-Gaskins D, Crosson S (2010) Interaction specificity, toxicity and regulation of a paralogous set of ParE/RelE-family toxin–antitoxin systems. Mol Microbiol 77:236–251. https://doi.org/10.1111/j.1365-2958.2010.07207.x
Filippidou S, Wunderlin T, Junier T, Jeanneret N, Dorador C, Molina V, Johnson D, Junier P (2016) A combination of extreme environmental conditions favor the prevalence of endospore-forming Firmicutes. Front Microbiol 7:1707. https://doi.org/10.3389/fmicb.2016.01707
Fishel R (2015) Mismatch repair. J Biol Chem 290(44):26395–26403. https://doi.org/10.1074/jbc.R115.660142
Fitzpatrick D, Walsh F (2016) Antibiotic resistance genes across a wide variety of metagenomes. FEMS Microbiol Ecol 92(2):1–8. https://doi.org/10.1093/femsec/fiv168
Fräre M, Rijks JQ, Rea J (1975) Estudio agroclimatológico de la zona andina. FAO, Roma
Frösler J, Panitz C, Wingender J, Flemming HC, Rettberg P (2017) Survival of Deinococcus geothermalis in biofilms under desiccation and simulated space and martian conditions. Astrobiology 17(5):431–447. https://doi.org/10.1089/ast.2015.1431
Galinski E, Trüper HG (1994) Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 15(2–3):95–108. https://doi.org/10.1111/j.1574-6976.1994.tb00128.x
Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62(9):1490–1499. https://doi.org/10.1016/j.chemosphere.2005.06.014
Girija KR, Sasikala Ch, Ramana ChV, Spröer C, Takaichi S, Thiel V, Imhoff JF (2010) Rhodobacter johrii sp. nov., an endospore-producing cryptic species isolated from semi-arid tropical soils. Int J Syst Evol Microbiol 60:2099–2107. https://doi.org/10.1099/ijs.0.011718-0
Giuliodori AM, Di Pietro F, Marzi S, Masquida B, Wagner R, Romby P, Gualerzi CP, Pon CL (2010) The cspA mRNA Is a thermosensor that modulates translation of the cold-shock protein CspA. Mol Cell 37(1):21–33. https://doi.org/10.1016/j.molcel.2009.11.033
Glaeser J, Klug G (2005) Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151(6):1927–1938. https://doi.org/10.1099/mic.0.27789-0
Glaeser J, Nuss AM, Berghoff BA, Klug G (2011) Singlet oxygen stress in microorganisms. Adv Microb Physiol 58:142–173. https://doi.org/10.1016/B978-0-12-381043-4.00004-0
Goh KM, Chan KG, Lim SW, Liew KJ, Chan CS, Shamsir MS, Ee R, Adrian TGS (2016) Genome analysis of a new Rhodothermaceae strain isolated from a hot spring. Front Microbiol 7:1109. https://doi.org/10.3389/fmicb.2016.01109
Gorriti MF, Dias GM, Chimetto LA, Trindade-Silva AE, Silva BS, Mesquita MM, Gregoracci GB, Farías ME, Thompson CC, Thompson FL (2014) Genomic and phenotypic attributes of novel Salinivibrios from stromatolites, sediment and water from a high altitude lake. BMC Genomics 15:473. https://doi.org/10.1186/1471-2164-15-473
Hacker J, Carniel E (2001) Ecological fitness, genomic islands and bacterial pathogenicity: a Darwinian view of the evolution of microbes. EMBO Rep 2:376–381. https://doi.org/10.1093/embo-reports/kve097
Harrison JJ, Ceri H, Turner RJ (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5(12):928–938. https://doi.org/10.1038/nrmicro1774
Hernández KL, Yannicelli B, Olsen LM, Dorador C, Menschel EJ, Molina V, Ramonsellez F, Hengst MB, Jeffrey WH (2016) Microbial activity response to solar radiation across contrasting environmental conditions in Salar de Huasco, Northern Chilean Altiplano. Front Microbiol 7:1857. https://doi.org/10.3389/fmicb.2016.01857
Hoffmann T, Bremer E (2011) Protection of Bacillus subtilis against cold stress via compatible-solute acquisition. J Bacteriol 193(7):1552–1562. https://doi.org/10.1128/JB.01319-10
Horiyama T, Nishino K (2014) AcrB, AcrD, and MdtABC multidrug efflux systems are involved in enterobactin export in Escherichia coli. PLoS ONE. https://doi.org/10.1371/journal.pone.0108642
Huang M, Hull CM (2017) Sporulation: how to survive on planet Earth (and beyond). Curr Genet 63(5):831–838. https://doi.org/10.1007/s00294-017-0694-7
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, Von Mering C, Bork P (2016) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:286–293. https://doi.org/10.1093/nar/gkv1248
Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11(7):443–454. https://doi.org/10.1038/nrmicro3032
Jamet A, Kiss E, Batut J, Puppo A, Hérouart D (2005) The kata catalase gene is regulated by OxyR in both free-living and symbiotic Sinorhizobium meliloti. J Bacteriol 187(1):376–381. https://doi.org/10.1128/JB.187.1.376-381.2005
Janion C (2008) Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli. Int J Biol Sc 4(6):338–344. https://doi.org/10.7150/ijbs.4.338
Kish A, Kirkali G, Robinson C, Rosenblatt R, Aruga J, Disdaroglu M et al (2009) Salt shiel: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ Microbiol 11(5):1066–1078. https://doi.org/10.1111/j.1462-2920.2008.01828.x
Korshunov SS, Imlay JA (2002) A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol Microbiol 43(1):95–106. https://doi.org/10.1046/j.1365-2958.2002.02719.x
Kress W, Maglica Z, Weber-Ban E (2009) Clp chaperone-protease: structure and function. Res Microbiol 160:618–628. https://doi.org/10.1016/j.resmic.2009.08.006
Kurth D, Belfiore C, Gorriti MF, Cortez N, Farias ME, Albarracín VH (2015) Genomic and proteomic evidences unravel the UV-resistome of the poly-extremophile Acinetobacter sp. Ver3. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00328
Kurth D, Amadio A, Ordoñez OF, Albarracín VH, Gärtner W, Farías ME (2017) Arsenic metabolism in high altitude modern stromatolites revealed by metagenomic analysis. Sci Rep 7(1):1024. https://doi.org/10.1038/s41598-017-00896-0
Lebre PH, De Maayer P, Cowan DA (2017) Xerotolerant bacteria: surviving through a dry spell. Nat Rev Microbiol 15(5):285–296. https://doi.org/10.1038/nrmicro.2017.16
Levina N, Tötemeyer S, Stokes NR, Louis P, Jones MA, Booth IR (1999) Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. EMBO J 18(7):1730–1737. https://doi.org/10.1093/emboj/18.7.1730
Levine RL, Mosoni L, Berlett BS, Stadtman ER (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93(26):15036–15040. https://doi.org/10.1073/pnas.93.26.15036
Li GM (2008) Mechanisms and functions of DNA mismatch repair. Cell Res 18:85–98. https://doi.org/10.1038/cr.2007.115
Li K, Hein S, Zou W, Klug G (2004) The glutathione-glutaredoxin system in Rhodobacter capsulatus: part of a complex regulatory network controlling defense against oxidative stress. J Bacteriol 186(20):6800–6808
Li T, Weng Y, Ma X, Tian B, Dai S, Jin Y, Liu M, Li J, Yu J, Hua Y (2017) Deinococcus radiodurans toxin–antitoxin MazEF-dr mediates cell death in response to DNA damage stress. Front Microbiol 8:1427. https://doi.org/10.3389/fmicb.2017.01427
Lucas-Lledó JI, Lynch M (2009) Evolution of mutation rates: phylogenomic analysis of the photolyase/cryptochrome family. Mol Biol Evol 26(5):1143–1153. https://doi.org/10.1093/molbev/msp029
Mao D, Grogan DW (2017) How a genetically stable extremophile evolves: modes of genome diversification in the archaeon Sulfolobus acidocaldarius. J Bacteriol. https://doi.org/10.1128/JB.00177-17
Martínez-del Campo A, Ballado T, Camarena L, Dreyfus G (2011) In Rhodobacter sphaeroides, chemotactic operon 1 regulates rotation of the flagellar system 2. J Bacteriol 193(23):6781–6786. https://doi.org/10.1128/JB.05933-11
Mattison K, Wilbur JS, So M, Brennan RG (2006) Structure of FitAB from Neisseria gonorrhoeae bound to DNA reveals a tetramer of toxin–antitoxin heterodimers containing pin domains and ribbon-helix–helix motifs. J Biol Chem 281(49):37942–37951. https://doi.org/10.1074/jbc.M605198200
Moeller R, Stackebrandt E, Reitz G, Berger T, Rettberg P, Doherty AJ et al (2007) Role of DNA repair by nonhomologous-end joining in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV, and ionizing radiation. J Bacteriol 189(8):3306–3311. https://doi.org/10.1128/JB.00018-07
Molina V, Hernández K, Dorador C, Eissler Y, Hengst M, Pérez V, Harrod C (2016) Bacterial active community cycling in response to solar radiation and their influence on nutrient changes in a high-altitude wetland. Front Microbiol 7:1823. https://doi.org/10.3389/fmicb.2016.01823
Monastiriakos SK, Doiron KMJ, Siponen MI, Cupples CG (2004) Functional interactions between the MutL and Vsr proteins of Escherichia coli are dependent on the N-terminus of Vsr. DNA Repair (Amst) 3(6):639–647. https://doi.org/10.1016/j.dnarep.2004.02.008
Park JS, Marr MT, Roberts JW (2002) E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109(6):757–767. https://doi.org/10.1016/S0092-8674(02)00769-9
Pérez V, Hengst M, Kurte L, Dorador C, Jeffrey WH, Wattiez R, Molina V, Matallana-Surget S (2017) Bacterial survival under extreme UV radiation: a comparative proteomics study of Rhodobacter sp., isolated from high altitude wetlands in Chile. Front Microbiol 8:1173. https://doi.org/10.3389/fmicb.2017.01173
Phadtare S (2004) Recent developments in bacterial cold-shock response. Curr Issues Mol Biol 6(2):125–136
Pichereau V, Pocard -A, Hamelin J, Blanco C, Bernard T (1998) Differential effects of dimethylsulfoniumpropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities. Appl Environ Microbiol 64:1420–1429
Pilonieta MC, Nagy TA, Jorgensen DR, Detweiler CS (2012) A glycine betaine importer limits Salmonella stress resistance and tissue colonization by reducing trehalose production. Mol Microbiol 84(2):296–309. https://doi.org/10.1111/j.1365-2958.2012.08022.x
Ram Y, Hadany L (2014) Stress-induced mutagenesis and complex adaptation. Proc Biol Sci B 281(1792):20141025. https://doi.org/10.1098/rspb.2014.1025
Rastogi RP, Richa Kumar A, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids. https://doi.org/10.4061/2010/592980
Riesenman PJ, Nicholson WL (2000) Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl Environ Microbiol 66(2):620–626. https://doi.org/10.1128/AEM.66.2.620-626.2000
Risacher F, Alonso H, Salazar C (1999) Geoquímica de aguas en cuencias cerradas: I, II y III regiones-Chile. Ministerio de Obras Públicas, Dirección general de Aguas, Santiago
Risacher F, Alonso H, Salazar C (2003) The origin of brines and salts in Chilean salars: a hydrochemical review. Earth-Sci Rev 63(3–4):249–293. https://doi.org/10.1016/S0012-8252(03)00037-0
Sancar A (2008) Structure and Function of Photolyase and in VivoEnzymology: 50th Anniversary. J Biol Chem 283(47):32153–32157. https://doi.org/10.1074/jbc.R800052200
Schnell S, Steinman HM (1995) Function and stationary-phase induction of periplasmic copper–zinc superoxide dismutase and catalase/peroxidase in Caulobacter crescentus. J Bacteriol 177(20):5924–5929. https://doi.org/10.1128/jb.177.20.5924-5929.1995
Seckbach J, Oren A, Stan-lotter H (2013) Polyextremophiles: life under multiple forms of stress. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6488-0
Sengupta S, Chattopadhyay MK, Grossart HP (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4:1–13. https://doi.org/10.3389/fmicb.2013.00047
Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75(1):133–191. https://doi.org/10.1128/MMBR.00015-10
Sleator RD, Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26(1):49–71. https://doi.org/10.1111/j.1574-6976.2002.tb00598.x
Storz G, Hengge R (2011) Bacterial stress responses. ASM Press, Washington, DC
Teitzel GM, Parsek MR (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol 69(4):2313–2320. https://doi.org/10.1128/AEM.69.4.2313
Tsuzuki M, Moskvin OV, Kuribayashi M, Sato K, Retamal S, Abo M et al (2011) Salt stress-induced changes in the transcriptome, compatible solutes, and membrane lipids in the facultatively phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 77(21):7551–7559. https://doi.org/10.1128/AEM.05463-11
Varin T, Lovejoy C, Jungblut AD, Vincent WF, Corbeil J (2012) Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the high Arctic. Appl Environ Microbiol 78(2):549–559. https://doi.org/10.1128/AEM.06354-11
Warner DF, Ndwandwe DE, Abrahams GL, Kana BD, Machowski EE, Venclovas Č, Mizrahi V (2010) Essential roles for imuA′- and imuB-encoded accessory factors in DnaE2-dependent mutagenesis in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 107(29):13093–13098. https://doi.org/10.1073/pnas.1002614107
Webb KM, DiRuggiero J (2012) Role of Mn2+ and compatible solutes in the radiation resistance of thermophilic bacteria and archaea. Archaea. https://doi.org/10.1155/2012/845756
Weber MHW, Klein W, Müller L, Niess UM, Marahiel MA (2001) Role of the Bacillus subtilis fatty acid desaturase in membrane adaptation during cold shock. Mol Microbiol 39(5):1321–1329. https://doi.org/10.1046/j.1365-2958.2001.02322.x
Wright GD (2007) The antibiotic resistome: the nexus of chemical and genetic diversity. Nat Rev Microbiol 5:175–186. https://doi.org/10.1038/nrmicro1614
Yamaguchi Y, Inouye M (2011) Regulation of growth and death in Escherichia coli by toxin–antitoxin systems. Nat Rev Microbiol 9(11):779–790. https://doi.org/10.1038/nrmicro2651
Ziegelhoffer EC, Donohue TJ (2009) Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7(12):856–863. https://doi.org/10.1038/nrmicro2237
Acknowledgements
We thank Juan Ugalde for support in bioinformatic analysis. We thank Jaime Guerrero, Pedro Luca, Margarita Luca for assistance during field trips.
Funding
This research was supported by Grants Fondecyt No. 1140179, No. 1140356 and CeBiB FB0001. Vilma Pérez is the recipient of a Conicyt PhD scholarship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table 1
Environmental resistome of Rhodobacter sp. Rb3. Genes encoding for proteins involved in each putative class of adaptation strategies to extreme environmental conditions. COG: Clusters of Orthologous Groups. Supplementary material 1 (DOC 570 kb)
Supplementary Table 2
Metabolic profile of Rhodobacter sp. Rb3. Supplementary material 2 (DOC 109 kb)
Rights and permissions
About this article
Cite this article
Pérez, V., Dorador, C., Molina, V. et al. Rhodobacter sp. Rb3, an aerobic anoxygenic phototroph which thrives in the polyextreme ecosystem of the Salar de Huasco, in the Chilean Altiplano. Antonie van Leeuwenhoek 111, 1449–1465 (2018). https://doi.org/10.1007/s10482-018-1067-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-018-1067-z