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Extremophiles

, Volume 22, Issue 3, pp 537–552 | Cite as

Draft genome sequences of bacteria isolated from the Deschampsia antarctica phyllosphere

  • Fernanda P. Cid
  • Fumito Maruyama
  • Kazunori Murase
  • Steffen P. Graether
  • Giovanni Larama
  • Leon A. Bravo
  • Milko A. Jorquera
Original Paper

Abstract

Genome analyses are being used to characterize plant growth-promoting (PGP) bacteria living in different plant compartiments. In this context, we have recently isolated bacteria from the phyllosphere of an Antarctic plant (Deschampsia antarctica) showing ice recrystallization inhibition (IRI), an activity related to the presence of antifreeze proteins (AFPs). In this study, the draft genomes of six phyllospheric bacteria showing IRI activity were sequenced and annotated according to their functional gene categories. Genome sizes ranged from 5.6 to 6.3 Mbp, and based on sequence analysis of the 16S rRNA genes, five strains were identified as Pseudomonas and one as Janthinobacterium. Interestingly, most strains showed genes associated with PGP traits, such as nutrient uptake (ammonia assimilation, nitrogen fixing, phosphatases, and organic acid production), bioactive metabolites (indole acetic acid and 1-aminocyclopropane-1-carboxylate deaminase), and antimicrobial compounds (hydrogen cyanide and pyoverdine). In relation with IRI activity, a search of putative AFPs using current bioinformatic tools was also carried out. Despite that genes associated with reported AFPs were not found in these genomes, genes connected to ice-nucleation proteins (InaA) were found in all Pseudomonas strains, but not in the Janthinobacterium strain.

Keywords

Antarctic bacteria Antifreeze proteins Ice recrystallization inhibition Deschampsia antarctica Phyllosphere Plant growth-promoting bacteria 

Notes

Acknowledgements

This study was financed with funds from Chilean Antarctic Institute-INACH (code RT_02_16), The National Fund for Scientific and Technological Development-FONDECYT (No. 1160302) and The National Commission for Scientific and Technological Research-CONICYT (Code USA2013-0010 and MEC no. 80140015). This work was supported by the Ministry of Education, Culture, Sports, Science and Technology in Japan or Japan Society for the Promotion of Science under Grants-in-Aid for Scientific Research (KAKENHI) (Grant Numbers 16H05830/16H05501/16H01782/16H02767); Kurita Water and Environment Foundation Grant; Ichiro Kanehara Foundation Scholarship Grant for Research in Basic Medical Sciences and Medical Care; Senri Life Science Foundation Kishimoto Grant; and Japan Agency for Medical Research and Development (AMED), and also by National Science and Engineering Research Council of Canada (NSERC). F. Cid thanks to the doctor scholarships awarded by INACH (Code DT_01-13), CONICYT (No. 21140534), MECESUP FRO1204 and La Frontera University.

Supplementary material

792_2018_1015_MOESM1_ESM.doc (1.2 mb)
Supplementary material 1 (DOC 1215 kb)

References

  1. Abe K, Watabe S, Emori Y, et al (1989) An ice nucleation active gene of Erwinia ananas. Sequence similarity to those of Pseudomonas species and regions required for ice nucleation activity. FEBS Lett 258:297–300.  https://doi.org/10.1016/0014-5793(89)81678-3 PubMedCrossRefGoogle Scholar
  2. Acuña JJ, Durán P, Lagos LM et al (2016) Bacterial alkaline phosphomonoesterase in the rhizospheres of plants grown in Chilean extreme environments. Biol Fertil Soils 52:763–773CrossRefGoogle Scholar
  3. Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedPubMedCentralCrossRefGoogle Scholar
  4. Andorfer CA, Duman JG (2000) Isolation and characterization of cDNA clones encoding antifreeze proteins of the pyrochroid beetle Dendroides canadensis. J Insect Physiol 46:365–372PubMedCrossRefGoogle Scholar
  5. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  6. Aziz RK, Bartels D, Best AA et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:1–15CrossRefGoogle Scholar
  7. Banerjee A, Bareh DA, Joshi SR (2017) Native microorganisms as potent bioinoculants for plant growth promotion in shifting agriculture (Jhum) systems. J Soil Sci Plant Nutr 17:127–140Google Scholar
  8. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:1–7Google Scholar
  9. Berlec A (2012) Novel techniques and findings in the study of plant microbiota: search for plant probiotics. Plant Sci 193–194:96–102PubMedCrossRefGoogle Scholar
  10. Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83CrossRefGoogle Scholar
  11. Blumer C, Haas D (2000) Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177PubMedCrossRefGoogle Scholar
  12. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:1–7CrossRefGoogle Scholar
  13. Brettin T, Davis JJ, Disz T et al (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brighigna L, Montaini P, Favilli F, Cabarez A (1992) Role of the nitrogen-fixing bacterial microflora in the epiphytism of Tillandsia (Bromeliaceae). Am J Bot 79:723–727CrossRefGoogle Scholar
  15. Bringel F, Couée I (2015) Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front Microbiol 6:1–14CrossRefGoogle Scholar
  16. Bruton BD, Wells JM, Lester GE, Patterson CL (1991) Pathogenicity and characterization of Erwinia ananas causing a postharvest disease of cantaloup fruit. Plant Dis 75:180–183CrossRefGoogle Scholar
  17. Burkovski A (2003) Ammonium assimilation and nitrogen control in Corynebacterium glutamicum and its relatives: an example for new regulatory mechanisms in actinomycetes. FEMS Microbiol Rev 27:617–628PubMedCrossRefGoogle Scholar
  18. Buysens S, Heungens K, Poppe J, Hofte M (1996) Involvement of pyochelin and pyoverdin in suppression of pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 62:865–871PubMedPubMedCentralGoogle Scholar
  19. Castro Jimenez J, Casal P, Gonzalez Gaya B et al (2014) Organophosphate ester (OPE) flame retardants and plasticizers in the open Mediterranean and Black seas atmosphere. Environ Sci Technol 76:364–367Google Scholar
  20. Chakrabartty A, Hew L, Shears M, Fletcher G (1988) Primary structures of the alanine-rich antifreeze polypeptides from grubby sculpin, Myoxocephalus aenaeus. Can J Zool 66:403–408CrossRefGoogle Scholar
  21. Cheng CHC, DeVries AL (1989) Structures of antifreeze peptides from the antarctic eel pout, Austrolycicthys brachycephalus. Biochim Biophys Acta 997:55–64PubMedCrossRefGoogle Scholar
  22. Cid FP, Inostroza NG, Graether SP et al (2016a) Bacterial community structures and ice recrystallization inhibition activity of bacteria isolated from the phyllosphere of the Antarctic vascular plant Deschampsia antarctica. Polar Biol 40:1319–1331CrossRefGoogle Scholar
  23. Cid FP, Rilling JI, Graether SP et al (2016b) Properties and biotechnological applications of ice binding proteins in bacteria. FEMS Microbiol Lett 363:1–12CrossRefGoogle Scholar
  24. Coil D, Jospin G, Darling A (2015) A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics 31:587–589PubMedCrossRefGoogle Scholar
  25. Cowan DA, Makhalanyane TP, Dennis PG, Hopkins DW (2014) Microbial ecology and biogeochemistry of continental antarctic soils. Front Microbiol 5:1–10CrossRefGoogle Scholar
  26. Daughton C, Cook A, Alexander M (1979) Bacterial conversion of alkylphosphonates to natural products via carbon-phosphorus bond cleavage. J Agric Food Chem 27:1375–1382CrossRefGoogle Scholar
  27. Davies PL (2016) Antarctic moss is home to many epiphytic bacteria that secrete antifreeze proteins. Environ Microbiol Rep 8:1–2PubMedCrossRefGoogle Scholar
  28. De Maayer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15:508–517PubMedPubMedCentralCrossRefGoogle Scholar
  29. Do H, Kim S-J, Kim H, Lee J (2014) Structure-based characterization and antifreeze properties of a hyperactive ice-binding protein from the Antarctic bacterium Flavobacterium frigoris PS1. Biol Crystallogr 70:1061–1073CrossRefGoogle Scholar
  30. El Amrani A, Dumas AS, Wick LY et al (2015) “Omics” Insights into PAH degradation toward improved green remediation biotechnologies. Environ Sci Technol 49:11281–11291PubMedCrossRefGoogle Scholar
  31. Ewart KV, Rubinsky B, Fletcher GL (1992) Structural and functional similarity between fish antifreeze proteins and calcium-dependent lectins. Biochem Biophys Res Commun 185:335–340PubMedCrossRefGoogle Scholar
  32. Fürnkranz M, Wanek W, Richter A et al (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–570PubMedCrossRefGoogle Scholar
  33. Garnham CP, Campbell RL, Davies PL (2011) Anchored clathrate waters bind antifreeze proteins to ice. Proc Natl Acad Sci USA 108:7363–7367PubMedPubMedCentralCrossRefGoogle Scholar
  34. Glick B (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15CrossRefGoogle Scholar
  35. Glick BR (2015) Beneficial plant-bacterial interactions. Springer, SwitzerlandCrossRefGoogle Scholar
  36. Graham LA, Davies PL (2005) Glycine-rich antifreeze proteins from snow fleas. Science 310:461PubMedCrossRefGoogle Scholar
  37. Graham LA, Liou Y, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388:727–728PubMedCrossRefGoogle Scholar
  38. Gronwald W, Loewen C, Lix B et al (1998) The solution structure of type II antifreeze protein reveals a new member of the lectin family. Biochemistry 37:4712–4721PubMedCrossRefGoogle Scholar
  39. Gwak IG, Sic Jung W, Kim HJ et al (2010) Antifreeze protein in antarctic marine diatom, Chaetoceros neogracile. Mar Biotechnol 12:630–639PubMedCrossRefGoogle Scholar
  40. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319PubMedCrossRefGoogle Scholar
  41. Hakim A, Nguyen JB, Basu K et al (2013) Crystal structure of an insect antifreeze protein and its implications for ice binding. J Biol Chem 288:12295–12304PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hashim NHF, Bharudin I, Nguong DLS et al (2013) Characterization of Afp1, an antifreeze protein from the psychrophilic yeast Glaciozyma antarctica PI12. Extremophiles 17:63–73PubMedCrossRefGoogle Scholar
  43. Hassan W, Hussain M, Bashir S et al (2015) ACC-deaminase and/or nitrogen fixing rhizobacteria and growth of wheat (Triticum aestivum L.). J Soil Sci Plant Nutr 15:232–248Google Scholar
  44. Hew CL, Wang NC, Yan S et al (1986) Biosynthesis of antifreeze polypeptides in the winter flounder. Characterization and seasonal occurrence of precursor polypeptides. Eur J Biochem FEBS 160:267–272CrossRefGoogle Scholar
  45. Hew CL, Wang NC, Joshi S et al (1988) Multiple genes provide the basis for antifreeze protein diversity and dosage in the ocean pout, Macrozoarces americanus. J Biol Chem 263:12049–12055PubMedGoogle Scholar
  46. Hoshino T, Kiriaki M, Ohgiya S et al (2003) Antifreeze proteins from snow mold fungi. Can J Bot 81:1175–1181CrossRefGoogle Scholar
  47. Huang X, Miller W (1991) A time-efficient, linear-space similarity algorithm. Adv Appl Math 357:337–357CrossRefGoogle Scholar
  48. Inostroza NG, Barra PJ, Wick LY et al (2016) Effect of rhizobacterial consortia from undisturbed arid- and agro-ecosystems on wheat growth under differing conditions. Lett Appl Microbiol 64:158–163CrossRefGoogle Scholar
  49. Jackson CR, Randolph KC, Osborn SL, Tyler HL (2013) Culture dependent and independent analysis of bacterial communities associated with commercial salad leaf vegetables. BMC Microbiol 13:274PubMedPubMedCentralCrossRefGoogle Scholar
  50. Janech MG, Krell A, Mock T et al (2006) Ice-binding proteins from sea ice diatoms (Bacillariophyceae)1. J Phycol 42:410–416CrossRefGoogle Scholar
  51. Johnson LS, Eddy SR, Portugaly E (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinf 11:431CrossRefGoogle Scholar
  52. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44CrossRefGoogle Scholar
  53. Jorquera MA, Shaharoona B, Nadeem SM et al (2012) Plant growth-promoting rhizobacteria associated with ancient clones of creosote bush (Larrea tridentata). Microb Ecol 64:1008–1017PubMedCrossRefGoogle Scholar
  54. Jorquera M, Inostroza N, Lagos L et al (2014) Bacterial community structure and detection of putative plant growth-promoting rhizobacteria associated with plants grown in Chilean agro-ecosystems and undisturbed ecosystems. Biol Fertil Soils 50:1141–1153CrossRefGoogle Scholar
  55. Jorquera MA, Maruyama F, Ogram AV et al (2016) Rhizobacterial community structures associated with native plants grown in Chilean extreme environments. Microb Ecol 72:1–14CrossRefGoogle Scholar
  56. Kandaswamy K, Chou K, Martinetz T et al (2011) AFP-Pred: a random forest approach for predicting antifreeze proteins from sequence-derived properties. J Theor Biol 270:56–62PubMedCrossRefGoogle Scholar
  57. Kido K, Adachi R, Masaru H, et al (2008) Internal fruit rot of netted melon caused by Pantoea ananatis (Erwinia ananas) in Japan. J Gen Plant Pathol 74:302–312CrossRefGoogle Scholar
  58. Kiko R (2010) Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer? Polar Biol 33:543–556CrossRefGoogle Scholar
  59. Kim SJ, Shin SC, Hong SG et al (2012) Genome sequence of Janthinobacterium sp. strain PAMC 25724, isolated from alpine glacier cryoconite. J Bacteriol 194:2096PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kondo H, Hanada Y, Sugimoto H et al (2012) Ice-binding site of snow mold fungus antifreeze protein deviates from structural regularity and high conservation. Proc Natl Acad Sci 109:9360–9365PubMedPubMedCentralCrossRefGoogle Scholar
  61. Koo H, Strope BM, Kim EH et al (2016) Draft genome sequence of Janthinobacterium sp. Ant5-2-1, isolated from proglacial lake Podprudnoye in the Schirmacher oasis of east Antarctica. Genome Announc 4:1–2CrossRefGoogle Scholar
  62. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1–5.  https://doi.org/10.1093/molbev/msw054 PubMedCrossRefGoogle Scholar
  63. Kwak M, Haeyoung J, Madhaiyan M et al (2014) Genome information of Methylobacterium oryzae, a plant-probiotic methylotroph in the phyllosphere. PLoS ONE 9:e106704PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kwan AHY, Fairley K, Anderberg PI et al (2005) Solution structure of a recombinant type I sculpin antifreeze protein. Biochemistry 44:1980–1988PubMedCrossRefGoogle Scholar
  65. Lagos ML, Maruyama F, Nannipieri P, et al (2015) Current overview on the study of bacteria in the rhizosphere by modern molecular techniques: a mini-review. J Soil Sci Plant Nutr 15:504–523.  https://doi.org/10.4067/S0718-95162015005000042 Google Scholar
  66. Lee JK, Kim HJ (2016) Cloning, expression, and activity of type IV antifreeze protein from cultured subtropical olive flounder (Paralichthys olivaceus). Fish Aquat Sci 19:1–7CrossRefGoogle Scholar
  67. Lee JK, Park KS, Park S et al (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228PubMedCrossRefGoogle Scholar
  68. Lee JH, Park AK, Do H et al (2012a) Structural basis for antifreeze activity of ice-binding protein from arctic yeast. J Biol Chem 287:11460–11468PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lee SG, Koh HY, Lee JH et al (2012b) Cryopreservative effects of the recombinant ice-binding protein from the arctic yeast Leucosporidium sp. on red blood cells. Appl Biochem Biotechnol 167:824–834PubMedCrossRefGoogle Scholar
  70. Li XM, Trinh KY, Hew CL et al (1985) Structure of an antifreeze polypeptide and its precursor from the ocean pout, Macrozoarces americanus. J Biol Chem 260:12904–12909PubMedGoogle Scholar
  71. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedPubMedCentralCrossRefGoogle Scholar
  72. Marshall C, Fletcher G, Davies P (2004) Hyperactive antifreeze protein in a fish. Nature 429:153PubMedCrossRefGoogle Scholar
  73. Martínez-Rosales C, Fullana N, Musto H, Castro-Sowinski S (2012) Antarctic DNA moving forward: genomic plasticity and biotechnological potential. FEMS Microbiol Lett 331:1–9PubMedCrossRefGoogle Scholar
  74. Martínez-Viveros O, Jorquera MA, Crowley DE et al (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319CrossRefGoogle Scholar
  75. Mayak S, Tirosh T, Glick BR (2014a) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefGoogle Scholar
  76. Mayak S, Tirosh T, Glick BR (2014b) Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci 166:525–530CrossRefGoogle Scholar
  77. Meyer K, Keil M, Naldrett M (1999) A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett 447:171–178PubMedCrossRefGoogle Scholar
  78. Michelsen CF, Stougaard P (2012) Hydrogen cyanide synthesis and antifungal activity of the biocontrol strain Pseudomonas fluorescens In5 from Greenland is highly dependent on growth medium. Can J Microbiol 58:381–390PubMedCrossRefGoogle Scholar
  79. Middleton AJ, Marshall CB, Faucher F et al (2012) Antifreeze protein from freeze-tolerant grass has a beta-roll fold with an irregularly structured ice-binding site. J Mol Biol 416:713–724PubMedCrossRefGoogle Scholar
  80. Miller AM, Figueiredo JEF, Linde GA, et al (2016) Characterization of the inaA gene and expression of ice nucleation phenotype in Pantoea ananatis isolates from maize white spot disease. Genet Mol Res 15:1–8.  https://doi.org/10.4238/gmr.15017863 Google Scholar
  81. Mindock CA, Petrova MA, Hollingsworth RI (2001) Re-evaluation of osmotic effects as a general adaptative strategy for bacteria in sub-freezing conditions. Biophys Chem 89:13–24PubMedCrossRefGoogle Scholar
  82. Mok YF, Lin FH, Graham LA et al (2010) Structural basis for the superior activity of the large isoform of snow flea antifreeze protein. Biochemistry 49:2593–2603PubMedCrossRefGoogle Scholar
  83. Mota MS, Gomes CB, Souza Júnior IT, Moura AB (2017) Bacterial selection for biological control of plant disease: criterion determination and validation. Brazil J Microbiol 48:62–70CrossRefGoogle Scholar
  84. Muryoi N, Sato M, Kaneko S et al (2004) Cloning and expression of afpA, a gene encoding an antifreeze protein from the arctic plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. J Bacteriol 186:5661–5671PubMedPubMedCentralCrossRefGoogle Scholar
  85. Nakamura K, Hiraishi A, Yoshimi Y et al (1995) Microlunatus phosphovorus gen. nov., sp. nov., a new gram-positive polyphosphate-accumulating bacterium isolated from activated sludge. Int J Syst Bacteriol 45:17–22PubMedCrossRefGoogle Scholar
  86. Ohnishi N, Maruyama F, Ogawa H et al (2014) Genome sequence of a Bacillus anthracis outbreak strain from Zambia, 2011. Genome Announc 2:1–2CrossRefGoogle Scholar
  87. Ortet P, Barakat M, Lalaouna D et al (2011) Complete genome sequence of a beneficial plant root-associated bacterium, Pseudomonas brassicacearum. J Bacteriol 193:3146PubMedPubMedCentralCrossRefGoogle Scholar
  88. Paulsen I, Press C, Ravel J et al (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 23:873–878PubMedCrossRefGoogle Scholar
  89. Pavlov MS, Lira F, Martínez JL et al (2015) Draft genome sequence of Antarctic Pseudomonas sp. strain KG01 with full potential for biotechnological applications. Genome Announc 3:9–10Google Scholar
  90. Perazzolli M, Antonielli L, Storari M et al (2014) Resilience of the natural phyllosphere microbiota of the grapevine to chemical and biological pesticides. Appl Environ Microbiol 80:3585–3596PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pihakaski-Maunsbach K, Moffatt B, Testillano P et al (2001) Genes encoding chitinase-antifreeze proteins are regulated by cold and expressed by all cell types in winter rye shoots. Physiol Plant 112:359–371PubMedCrossRefGoogle Scholar
  92. Qin W, Doucet D, Tyshenko MG, Walker VK (2007) Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Mol Biol 16:423–434PubMedCrossRefGoogle Scholar
  93. Raja P, Balachandar D, Sundaram SP (2008) PCR fingerprinting for identification and discrimination of plant-associated facultative methylobacteria. Indian J Biotechnol 7:508–514Google Scholar
  94. Rastogi G, Coaker GL, Leveau JHJ (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10PubMedCrossRefGoogle Scholar
  95. Raymond JA (2015) Dependence on epiphytic bacteria for freezing protection in an Antarctic moss, Bryum argenteum. Environ Microbiol Rep 8:14–19PubMedCrossRefGoogle Scholar
  96. Raymond JA, Fritsen C, Shen K (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol Ecol 61:214–221PubMedCrossRefGoogle Scholar
  97. Raymond JA, Christner BC, Schuster SC (2008) A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12:713–717PubMedCrossRefGoogle Scholar
  98. Reetha AK, Pavani SL, Mohan S (2014) Hydrogen cyanide production ability by bacterial antagonist and their antibiotics inhibition potential on Macrophomina phaseolina (Tassi.) Goid. Int J Curr Microbiol Appl Sci 3:172–178Google Scholar
  99. Rodríguez-Rojas F, Tapia P, Castro-Nallar E et al (2016) Draft genomes sequence of a multi-metal resistant bacterium Pseudomonas putida ATH-43 isolated from Greenwich island, Antarctica. Front Microbiol 7:1–5CrossRefGoogle Scholar
  100. Scott GK, Davies PL, Shears MA, Fletcher GL (1987) Structural variations in the alanine-rich antifreeze proteins of the pleuronectinae. Eur J Biochem 168:629–633PubMedCrossRefGoogle Scholar
  101. Scott GK, Hayes PH, Fletcher GL, Davies PL (1988) Wolffish antifreeze protein genes are primarily organized as tandem repeats that each contain two genes in inverted orientation. Mol Cell Biol 8:3670–3675PubMedPubMedCentralCrossRefGoogle Scholar
  102. See-Too W, Lim Y, Ee R et al (2016) Complete genome of Pseudomonas sp. strain L10.10, a psychrotolerant biofertilizer that could promote plant growth. J Biotechnol 222:84–85PubMedCrossRefGoogle Scholar
  103. Shoemaker WR, Muscarella ME, Lennon JT (2015) Genome sequence of the soil bacterium Jantinobacterium sp. KBS0711. Genome Announc 3:e00689–15PubMedPubMedCentralCrossRefGoogle Scholar
  104. Singh RN, Gaba S, Yadav AN et al (2016) First high quality draft genome sequence of a plant growth promoting and cold active enzyme producing psychrotrophic Arthrobacter agilis strain L77. Stand Genomic Sci 11:1–9CrossRefGoogle Scholar
  105. Sonnhammer EL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins Struct Funct Genet 28:405–420PubMedCrossRefGoogle Scholar
  106. Sönnichsen FD, DeLuca CI, Davies PL, Sykes BD (1996) Refined solution structure of type III antifreeze protein: hydrophobic groups may be involved in the energetics of the protein-ice interaction. Structure 4:1325–1337PubMedCrossRefGoogle Scholar
  107. Sun X, Griffith M, Pasternak JJ, Glick BR (1995) Low temperature growth, freezing survival, and production of antifreeze protein by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 41:776–784PubMedCrossRefGoogle Scholar
  108. Suyal DC, Shukla A, Goel R (2014) Growth promotory potential of the cold adapted diazotroph Pseudomonas migulae S10724 against native green gram (Vigna radiata (L.) Wilczek). 3. Biotech 4:665–668Google Scholar
  109. Teixeira LCRS, Peixoto RS, Cury JC et al (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001PubMedCrossRefGoogle Scholar
  110. Verma P, Yadav AN, Su K et al (2016) Molecular diversity and multifarious plant growth promoting attributes of Bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58PubMedCrossRefGoogle Scholar
  111. Viscardi S, Ventorino V, Duran P et al (2016) Assessment of plant growth promoting activities and abiotic stress tolerance of Azotobacter chroococcum strains for a potential use in sustainable agriculture. J Soil Sci Plant Nutr 16:848–863Google Scholar
  112. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefGoogle Scholar
  113. Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174PubMedPubMedCentralCrossRefGoogle Scholar
  114. Wang W, Zhang S, Zhou Y et al (2016) Synthesis and herbicidal activity of α-(substituted phenoxybutyryloxy or valeryloxy) alkylphosphonates and 2-(substituted phenoxybutyryloxy) alkyl-5,5-dimethyl-1,3,2-dioxaphosphinan-2-one. J Agric Food Chem 64:6911–6915PubMedCrossRefGoogle Scholar
  115. Wheeler TJ, Eddy SR (2013) Nhmmer: DNA homology search with profile HMMs. Bioinformatics 29:2487–2489PubMedPubMedCentralCrossRefGoogle Scholar
  116. Xiao X, Hui M, Liu Z (2016) iAFP-Ense: an ensemble classifier for identifying antifreeze protein by incorporating grey model and PSSM into PseAAC. J Membr Biol 249:845–854PubMedCrossRefGoogle Scholar
  117. Xu H, Griffith M, Patten CL, Glick BR (1998) Isolation and characterization of an antifreeze protein with ice nucleation activity from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 44:64–73CrossRefGoogle Scholar
  118. Yadav AN, Sachan SP, Verma P et al (2015) Culturable diversity and functional annotation of psychrotrophic bacteria from cold desert of Leh Ladakh (India). World J Microbiol Biotechnol 31:95–108PubMedCrossRefGoogle Scholar
  119. Yang C, Crowley DE, Borneman J, Keen N (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci 98:3889–3894PubMedPubMedCentralCrossRefGoogle Scholar
  120. Yoon S, Cruz-García C, Sanford R et al (2015) Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO3(−)/NO2(−) reduction pathways in Shewanella loihica strain PV-4. ISME J 9:11093–11104CrossRefGoogle Scholar
  121. Zhao Z, Deng G, Lui Q, Laursen RA (1998) Cloning and sequencing of cDNA encoding the LS-12 antifreeze protein in the longhorn sculpin, Myoxocephalus octodecimspinosis. Biochim Biophys Acta 1382:177–180PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Fernanda P. Cid
    • 1
    • 7
    • 8
  • Fumito Maruyama
    • 2
    • 3
  • Kazunori Murase
    • 2
  • Steffen P. Graether
    • 4
  • Giovanni Larama
    • 5
  • Leon A. Bravo
    • 6
    • 7
  • Milko A. Jorquera
    • 7
    • 8
  1. 1.Programa de Doctorado en Ciencias de Recursos NaturalesUniversidad de La FronteraTemucoChile
  2. 2.Department of Microbiology, Graduate School of MedicineKyoto UniversityKyotoJapan
  3. 3.The Japan Science and Technology Agency/Japan International Cooperation Agency, Science and Technology Research Partnership for Sustainable Development (JST/JICA, SATREPS)TokyoJapan
  4. 4.Department of Molecular and Cellular BiologyUniversity of GuelphGuelphCanada
  5. 5.Department of Mathematical EngineeringUniversidad de La FronteraTemucoChile
  6. 6.Departamento de Ciencias Agronómicas y Recursos Naturales, Facultad de Ciencias Agropecuarias y ForestalesUniversidad de la FronteraTemucoChile
  7. 7.Scientific and Technological Bioresource NucleusUniversidad de La FronteraTemucoChile
  8. 8.Applied Microbial Ecology Laboratory, Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y CienciasUniversidad de La FronteraTemucoChile

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