Applied Microbiology and Biotechnology

, Volume 103, Issue 7, pp 2857–2871 | Cite as

Psychrophilic lifestyles: mechanisms of adaptation and biotechnological tools

  • Tony CollinsEmail author
  • Rosa Margesin


Cold-adapted microorganisms inhabiting permanently low-temperature environments were initially just a biological curiosity but have emerged as rich sources of numerous valuable tools for application in a broad spectrum of innovative technologies. To overcome the multiple challenges inherent to life in their cold habitats, these microorganisms have developed a diverse array of highly sophisticated synergistic adaptations at all levels within their cells: from cell envelope and enzyme adaptation, to cryoprotectant and chaperone production, and novel metabolic capabilities. Basic research has provided valuable insights into how these microorganisms can thrive in their challenging habitat conditions and into the mechanisms of action of the various adaptive features employed, and such insights have served as a foundation for the knowledge-based development of numerous novel biotechnological tools. In this review, we describe the current knowledge of the adaptation strategies of cold-adapted microorganisms and the biotechnological perspectives and commercial tools emerging from this knowledge. Adaptive features and, where possible, applications, in relation to membrane fatty acids, membrane pigments, the cell wall peptidoglycan layer, the lipopolysaccharide component of the outer cell membrane, compatible solutes, antifreeze and ice-nucleating proteins, extracellular polymeric substances, biosurfactants, chaperones, storage materials such as polyhydroxyalkanoates and cyanophycins and metabolic adjustments are presented and discussed.


Psychrophiles Cell envelope Cryoprotection Enzymes Chaperones Metabolic adjustments 



All the technical staff at the CBMA are thanked for their skilful technical assistance. The Fundação para a Ciência e a Tecnologia (FCT), the European Social Fund (ESF), the Programa Operacional Potencial Humano (POPH) and the European Regional Development Fund (ERDF) are thanked for funding. 

Funding information

T.C. is supported by the FCT, the ESF, POPH, and the Investigador FCT Programme (IF/01635/2014). Funding by the ERDF is through project EcoAgriFood (NORTE-01-0145-FEDER-000009) via the North Portugal Regional Operational Programme (NORTE 2020) under the PORTUGAL 2020 Partnership Agreement. FCT funding was through the project EngXyl (EXPL/BBB-BIO/1772/2013-FCOMP-01-0124-FEDER-041595) and the strategic programme UID/BIA/04050/2019 at the CBMA.

Compliance with ethical standards

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Amaretti A, Raimondi S, Sala M, Roncaglia L, De Lucia M, Leonardi A, Rossi M (2010) Single cell oils of the cold-adapted oleaginous yeast Rhodotorula glacialis DBVPG 4785. Microb Cell Factories 9:73–76. Google Scholar
  2. Arcus VL, Prentice EJ, Hobbs JK, Mulholland AJ, Van der Kamp MW, Pudney CR, Parker EJ, Schipper LA (2016) On the temperature dependence of enzyme-catalyzed rates. Biochemistry 55(12):1681–1688. Google Scholar
  3. Arora A, Cameotra SS, Kumar R, Balomajumder C, Singh AK, Santhakumari B, Kumar P, Laik S (2016) Biosurfactant as a promoter of methane hydrate formation: thermodynamic and kinetic studies. Sci Rep 6:20893. Google Scholar
  4. Arrhenius S (1889) Uber die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Sauren. Z Phys Chem 4:226–248Google Scholar
  5. Avila C (2016) Biological and chemical diversity in Antarctica: from new species to new natural products. Biodiversity 17(1–2):5–11. Google Scholar
  6. Ayala-del-Río HL, Chain PS, Grzymski JJ, Ponder MA, Ivanova N, Bergholz PW, Di Bartolo G, Hauser L, Land M, Bakermans C, Rodrigues D, Klappenbach J, Zarka D, Larimer F, Richardson P, Murray A, Thomashow M, Tiedje JM (2010) The genome sequence of Psychrobacter arcticus 273-4, a psychroactive Siberian permafrost bacterium, reveals mechanisms for adaptation to low-temperature growth. Appl Environ Microbiol 76(7):2304–2312. Google Scholar
  7. Bajaj S, Singh DK (2015) Biodegradation of persistent organic pollutants in soil, water and pristine sites by cold-adapted microorganisms: mini review. Int Biodeterior Biodegrad 100:98–105. Google Scholar
  8. Bakermans C, Tollaksen SL, Giometti CS, Wilkerson C, Tiedje JM, Thomashow MF (2007) Proteomic analysis of Psychrobacter cryohalolentis K5 during growth at subzero temperatures. Extremophiles 11(2):343–354. Google Scholar
  9. Bar Dolev M, Bernheim R, Guo S, Davies PL, Braslavsky I (2016a) Putting life on ice: bacteria that bind to frozen water. J R Soc Interface 13(121).
  10. Bar Dolev M, Braslavsky I, Davies PL (2016b) Ice-binding proteins and their function. Annu Rev Biochem 85:515–542. Google Scholar
  11. Barauna RA, Freitas DY, Pinheiro JC, Folador AR, Silva A (2017) A proteomic perspective on the bacterial adaptation to cold: integrating OMICs data of the psychrotrophic bacterium Exiguobacterium antarcticum B7. Proteomes 5(1).
  12. Barroca M, Santos G, Gerday C, Collins T (2017a) Biotechnological aspects of cold-active enzymes. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 461–475Google Scholar
  13. Barroca M, Santos G, Johansson B, Gillotin F, Feller G, Collins T (2017b) Deciphering the factors defining the pH-dependence of a commercial glycoside hydrolase family 8 enzyme. Enzym Microb Technol 96:163–169. Google Scholar
  14. Benforte FC, Colonnella MA, Ricardi MM, Solar Venero EC, Lizarraga L, Lopez NI, Tribelli PM (2018) Novel role of the LPS core glycosyltransferase WapH for cold adaptation in the Antarctic bacterium Pseudomonas extremaustralis. PLoS One 13(2):e0192559. Google Scholar
  15. Borchert E, Jackson SA, O’Gara F, Dobson ADW (2016) Diversity of natural product biosynthetic genes in the microbiome of the deep sea sponges Inflatella pellicula, Poecillastra compressa, and Stelletta normani. Front Microbiol 7(1027).
  16. Borchert E, Jackson SA, O’Gara F, Dobson ADW (2017) Psychrophiles as a source of novel antimicrobials. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 527–540Google Scholar
  17. Bowman JP (2017) Genomics of psychrophilic bacteria and archaea. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 345–387Google Scholar
  18. Carillo S, Pieretti G, Parrilli E, Tutino ML, Gemma S, Molteni M, Lanzetta R, Parrilli M, Corsaro MM (2011) Structural investigation and biological activity of the lipooligosaccharide from the psychrophilic bacterium Pseudoalteromonas haloplanktis TAB 23. Chemistry 17(25):7053–7060. Google Scholar
  19. Carillo S, Pieretti G, Lindner B, Parrilli E, Filomena S, Tutino ML, Lanzetta R, Parrilli M, Corsaro MM (2013) Structural characterization of the core oligosaccharide isolated from the lipopolysaccharide of the psychrophilic bacterium Colwellia psychrerythraea strain 34H. Eur J Org Chem 2013(18):3771–3779. Google Scholar
  20. Caruso C, Rizzo C, Mangano S, Poli A, Di Donato P, Finore I, Nicolaus B, Di Marco G, Michaud L, Lo Giudice A (2018) Production and biotechnological potential of extracellular polymeric substances from sponge-associated Antarctic bacteria. Appl Environ Microbiol 84(4).
  21. Casillo A, Parrilli E, Sannino F, Mitchell DE, Gibson MI, Marino G, Lanzetta R, Parrilli M, Cosconati S, Novellino E, Randazzo A, Tutino ML, Corsaro MM (2017a) Structure-activity relationship of the exopolysaccharide from a psychrophilic bacterium: a strategy for cryoprotection. Carbohydr Polym 156:364–371. Google Scholar
  22. Casillo A, Ziaco M, Lindner B, Parrilli E, Schwudke D, Holgado A, Verstrepen L, Sannino F, Beyaert R, Lanzetta R, Tutino ML, Corsaro MM (2017b) Unusual lipid A from a cold-adapted bacterium: detailed structural characterization. ChemBioChem 18(18):1845–1854. Google Scholar
  23. Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S (1997) Carotenoid pigments of an Antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem Biophys Res Commun 239(1):85–90. Google Scholar
  24. Chen GQ (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38(8):2434–2446. Google Scholar
  25. Chintalapati S, Kiran MD, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol (Noisy-le-Grand) 50(5):631–642Google Scholar
  26. Ciesielski S, Górniak D, Możejko J, Świątecki A, Grzesiak J, Zdanowski M (2014) The diversity of bacteria isolated from Antarctic freshwater reservoirs possessing the ability to produce polyhydroxyalkanoates. Curr Microbiol 69(5):594–603. Google Scholar
  27. Cochet N, Widehem P (2000) Ice crystallization by Pseudomonas syringae. Appl Microbiol Biotechnol 54(2):153–161Google Scholar
  28. Colliec Jouault S, Chevolot L, Helley D, Ratiskol J, Bros A, Sinquin C, Roger O, Fischer A-M (2001) Characterization, chemical modifications and in vitro anticoagulant properties of an exopolysaccharide produced by Alteromonas infernus. Biochim Biophys Acta Gen Subj 1528(2):141–151. Google Scholar
  29. Collins T, Gerday C (2017) Enzyme catalysis in psychrophiles. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 209–235Google Scholar
  30. Collins T, Claverie P, D’Amico S, Georlette D, Gratia E, Hoyoux A, Meuwis MA, Poncin J, Sonan G, Feller G, Gerday C (2002a) Life in the cold: psychrophilic enzymes. In: Pandalai SG (ed) Recent research developments in proteins, vol 1. Transworld Research Network, Trivandrum, pp 13–26Google Scholar
  31. Collins T, Meuwis MA, Stals I, Claeyssens M, Feller G, Gerday C (2002b) A novel family 8 xylanase, functional and physicochemical characterization. J Biol Chem 277(38):35133–35139. Google Scholar
  32. Collins T, Hoyoux A, Dutron A, Georis J, Genot B, Dauvrin T, Arnaut F, Gerday C, Feller G (2006) Use of glycoside hydrolase family 8 xylanases in baking. JCS 43:79–84Google Scholar
  33. Collins T, Feller G, Gerday C, Meuwis MA (2012) Family 8 enzymes with xylanolytic activity. US Granted Patent US8309336 B2Google Scholar
  34. Corsaro MM, Piaz FD, Lanzetta R, Parrilli M (2002) Lipid A structure of Pseudoalteromonas haloplanktis TAC 125: use of electrospray ionization tandem mass spectrometry for the determination of fatty acid distribution. J Mass Spectrom 37(5):481–488. Google Scholar
  35. Corsaro MM, Casillo A, Parrilli E, Tutino ML (2017) Molecular structure of lipopolysaccharides of cold-adapted bacteria. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 285–303Google Scholar
  36. D’Amico S, Claverie P, Collins T, Feller G, Georlette D, Gratia E, Hoyoux A, Meuwis MA, Zecchinon L, Gerday C (2001) Cold-adapted enzymes: an unachieved symphony. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress, vol 2, protein adaptations and signal transduction, vol 3. Elsevier, Amsterdam, pp 31–42Google Scholar
  37. D’Amico S, Marx JC, Gerday C, Feller G (2003) Activity-stability relationships in extremophilic enzymes. J Biol Chem 278(10):7891–7896Google Scholar
  38. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7(4):385–389Google Scholar
  39. De Maayer P, Anderson D, Cary C, Cowan DA (2014) Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep 15(5):508–517. Google Scholar
  40. Deming JW, Young JN (2017) The role of exopolysaccharides in microbial adaptation to cold habitats. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, Cham, pp 259–284Google Scholar
  41. Dieser M, Greenwood M, Foreman CM (2010) Carotenoid pigmentation in Antarctic heterotrophic bacteria as a strategy to withstand environmental stresses. Arct Antarct Alp Res 42(4):396–405. Google Scholar
  42. Duchaud E, Boussaha M, Loux V, Bernardet J-F, Michel C, Kerouault B, Mondot S, Nicolas P, Bossy R, Caron C, Bessières P, Gibrat J-F, Claverol S, Dumetz F, Hénaff ML, Benmansour A (2007) Complete genome sequence of the fish pathogen Flavobacterium psychrophilum. Nat Biotechnol 25:763–769. Google Scholar
  43. Duman JG, Bennett V, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50(4):259–266. Google Scholar
  44. Dutron A, Georis J, Genot B, Dauvrin T, Collins T, Hoyoux A, Feller G (2012) Use of family 8 enzymes with xylanolytic activity in baking. US Granted Patent US8192772Google Scholar
  45. Ewert M, Deming JW (2013) Sea ice microorganisms: environmental constraints and extracellular responses. Biology 2(2):603–628. Google Scholar
  46. Feng S, Powell SM, Wilson R, Bowman JP (2014) Extensive gene acquisition in the extremely psychrophilic bacterial species Psychroflexus torquis and the link to sea-ice ecosystem specialism. Genome Biol Evol 6(1):133–148. Google Scholar
  47. Ferrer M, Chernikova TN, Yakimov MM, Golyshin PN, Timmis KN (2003) Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21:1266–1267. Google Scholar
  48. Fields PA, Dong Y, Meng X, Somero GN (2015) Adaptations of protein structure and function to temperature: there is more than one way to ‘skin a cat’. J Exp Biol 218(Pt 12):1801–1811. Google Scholar
  49. Fonseca F, Meneghel J, Cenard S, Passot S, Morris GJ (2016) Determination of intracellular vitrification temperatures for unicellular microorganisms under conditions relevant for cryopreservation. PLoS One 11(4):e0152939. Google Scholar
  50. Forster J (1887) Ueber einige Eigenschaften leuchtender Bakterien. Centr Bakteriol Parasitenk 2:337–340Google Scholar
  51. Frank S, Schmidt F, Klockgether J, Davenport CF, Gesell Salazar M, Volker U, Tummler B (2011) Functional genomics of the initial phase of cold adaptation of Pseudomonas putida KT2440. FEMS Microbiol Lett 318(1):47–54. Google Scholar
  52. Frommeyer M, Wiefel L, Steinbüchel A (2016) Features of the biotechnologically relevant polyamide family “cyanophycins” and their biosynthesis in prokaryotes and eukaryotes. Crit Rev Biotechnol 36(1):153–164. Google Scholar
  53. Gaiteri JC, Henley WH, Siegfried NA, Linz TH, Ramsey JM (2017) Use of ice-nucleating proteins to improve the performance of freeze–thaw valves in microfluidic devices. Anal Chem 89(11):5998–6005. Google Scholar
  54. Gao H, Yang ZK, Wu L, Thompson DK, 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. J Bacteriol 188(12):4560–4569. Google Scholar
  55. Gerday C (2013) Psychrophily and catalysis. Biology 2(2):719–741. Google Scholar
  56. Gesheva V, Stackebrandt E, Vasileva-Tonkova E (2010) Biosurfactant production by halotolerant Rhodococcus fascians from Casey station, Wilkes Land, Antarctica. Curr Microbiol 61(2):112–117. Google Scholar
  57. Ghobakhlou A-F, Johnston A, Harris L, Antoun H, Laberge S (2015) Microarray transcriptional profiling of Arctic Mesorhizobium strain N33 at low temperature provides insights into cold adaption strategies. BMC Genomics 16(1):383. Google Scholar
  58. Godin-Roulling A, Schmidpeter PAM, Schmid FX, Feller G (2015) Functional adaptations of the bacterial chaperone trigger factor to extreme environmental temperatures. EnvironMicrobiol 17(7):2407–2420. Google Scholar
  59. Goh YS, Tan IKP (2012) Polyhydroxyalkanoate production by Antarctic soil bacteria isolated from Casey Station and Signy Island. Microbiol Res 167(4):211–219. Google Scholar
  60. Goordial J, Raymond-Bouchard I, Zolotarov Y, de Bethencourt L, Ronholm J, Shapiro N, Woyke T, Stromvik M, Greer CW, Bakermans C, Whyte L (2016) Cold adaptive traits revealed by comparative genomic analysis of the eurypsychrophile Rhodococcus sp. JG3 isolated from high elevation McMurdo Dry Valley permafrost, Antarctica. FEMS Microbiol Ecol 92(2).
  61. He J, Yang Z, Hu B, Ji X, Wei Y, Lin L, Zhang Q (2015) Correlation of polyunsaturated fatty acids with the cold adaptation of Rhodotorula glutinis. Yeast 32(11):683–690. Google Scholar
  62. Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K, Rao CM, Shivaji S (2000) Carotenoids of an Antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch Microbiol 173(5–6):418–424Google Scholar
  63. Jung HC, Lebeault JM, Pan JG (1998) Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae. Nat Biotechnol 16(6):576–580. Google Scholar
  64. Kirk O, Christensen MW (2002) Lipases from Candida antarctica: unique biocatalysts from a unique origin. Org Process Res Dev 6(4):446–451. Google Scholar
  65. Kirti K, Amita S, Priti S, Mukesh Kumar A, Jyoti S (2014) Colorful world of microbes: carotenoids and their applications. Adv Biol 2014:13. Google Scholar
  66. Kitamoto D, Yanagishita H, Endo A, Nakaiwa M, Nakane T, Akiya T (2001) Remarkable antiagglomeration effect of a yeast biosurfactant, diacylmannosylerythritol, on ice-water slurry for cold thermal storage. Biotechnol Prog 17(2):362–365. Google Scholar
  67. Koh HY, Park H, Lee JH, Han SJ, Sohn YC, Lee SG (2017) Proteomic and transcriptomic investigations on cold-responsive properties of the psychrophilic Antarctic bacterium Psychrobacter sp. PAMC 21119 at subzero temperatures. Environ Microbiol 19(2):628–644. Google Scholar
  68. Krembs C, Eicken H, Deming JW (2011) Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc Natl Acad Sci U S A 108(9):3653–3658. Google Scholar
  69. Kumar A, Rao KM, Han SS (2018) Application of xanthan gum as polysaccharide in tissue engineering: a review. Carbohydr Polym 180:128–144. Google Scholar
  70. Leroy F, De Vuyst L (2016) Advances in production and simplified methods for recovery and quantification of exopolysaccharides for applications in food and health. J Dairy Sci 99(4):3229–3238. Google Scholar
  71. Li J, Izquierdo MP, Lee T-C (1997) Effects of ice-nucleation active bacteria on the freezing of some model food systems. Int J Food Sci Technol 32(1):41–49. Google Scholar
  72. Lim J, Thomas T, Cavicchioli R (2000) Low temperature regulated DEAD-box RNA helicase from the Antarctic archaeon, Methanococcoides burtonii. J Mol Biol 297(3):553–567Google Scholar
  73. Lonhienne T, Gerday C, Feller G (2000) Psychrophilic enzymes: revisiting the thermodynamic parameters of activation may explain local flexibility. Biochim Biophys Acta 1543(1):1–10Google Scholar
  74. López NI, Pettinari MJ, Stackebrandt E, Tribelli PM, Põtter M, Steinbüchel A, Méndez BS (2009) Pseudomonas extremaustralis sp. nov., a poly(3-hydroxybutyrate) producer isolated from an Antarctic environment. Curr Microbiol 59(5):514–519. Google Scholar
  75. Lorv JS, Rose DR, Glick BR (2014) Bacterial ice crystal controlling proteins. Scientifica 2014:976895. Google Scholar
  76. Madihalli C, Sudhakar H, Doble M (2016) Mannosylerythritol lipid-A as a pour point depressant for enhancing the low-temperature fluidity of biodiesel and hydrocarbon fuels. Energy Fuel 30(5):4118–4125. Google Scholar
  77. Makled SO, Hamdan AM, El-Sayed A-FM, Hafez EE (2017) Evaluation of marine psychrophile, Psychrobacter namhaensis SO89, as a probiotic in Nile tilapia (Oreochromis niloticus) diets. Fish Shellfish Immunol 61:194–200. Google Scholar
  78. Malavenda R, Rizzo C, Michaud L, Gerçe B, Bruni V, Syldatk C, Hausmann R, Lo Giudice A (2015) Biosurfactant production by Arctic and Antarctic bacteria growing on hydrocarbons. Polar Biol 38(10):1565–1574. Google Scholar
  79. Margesin R (2017) Psychrophiles: from biodiversity to biotechnology, 2nd edn. Springer, ChamGoogle Scholar
  80. Margesin R, Collins T (2019) Microbial ecology of the cryosphere (glacial and permafrost habitats): current knowledge. Appl Microbiol Biotechnol.
  81. Marx JG, Carpenter SD, Deming JW (2009) Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can J Microbiol 55(1):63–72. Google Scholar
  82. Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D’Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EP, Rouy Z, Sekowska A, Tutino ML, Vallenet D, von Heijne G, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15(10):1325–1335Google Scholar
  83. Methé BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci U S A 102(31):10913–10918. Google Scholar
  84. Miyake R, Kawamoto J, Wei Y-L, Kitagawa M, Kato I, Kurihara T, Esaki N (2007) Construction of a low-temperature protein expression system using a cold-adapted bacterium, Shewanella sp. strain Ac10, as the host. Appl Environ Microbiol 73(15):4849–4856. Google Scholar
  85. More TT, Yadav JSS, Yan S, Tyagi RD, Surampalli RY (2014) Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manag 144:1–25. Google Scholar
  86. Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NPA (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Biol Rev 70(1):222–252. Google Scholar
  87. Muñoz PA, Márquez SL, González-Nilo FD, Márquez-Miranda V, Blamey JM (2017) Structure and application of antifreeze proteins from Antarctic bacteria. Microb Cell Factories 16:138. Google Scholar
  88. Muralidharan J, Jayachandran S (2003) Physicochemical analyses of the exopolysaccharides produced by a marine biofouling bacterium, Vibrio alginolyticus. Process Biochem 38(6):841–847. Google Scholar
  89. Mykytczuk NCS, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:1211–1226. Google Scholar
  90. Nishida T, Morita N, Yano Y, Orikasa Y, Okuyama H (2007) The antioxidative function of eicosapentaenoic acid in a marine bacterium, Shewanella marinintestina IK-1. FEBS Lett 581(22):4212–4216. Google Scholar
  91. Ochsenreither K, Gluck C, Stressler T, Fischer L, Syldatk C (2016) Production strategies and applications of microbial single cell oils. Front Microbiol 7:1539. Google Scholar
  92. Okuyama H, Orikasa Y, Nishida T (2008) Significance of antioxidative functions of eicosapentaenoic and docosahexaenoic acids in marine microorganisms. Appl Environ Microbiol 74(3):570–574. Google Scholar
  93. Oswald VF, Chen W, Harvilla PB, Magyar JS (2014) Overexpression, purification, and enthalpy of unfolding of ferricytochrome c552 from a psychrophilic microorganism. J Inorg Biochem 131:76–78. Google Scholar
  94. Pandey R, Usui K, Livingstone RA, Fischer SA, Pfaendtner J, Backus EHG, Nagata Y, Fröhlich-Nowoisky J, Schmüser L, Mauri S, Scheel JF, Knopf DA, Pöschl U, Bonn M, Weidner T (2016) Ice-nucleating bacteria control the order and dynamics of interfacial water. Sci Adv 2(4).
  95. Pandey N, Jain R, Pandey A, Tamta S (2018) Optimisation and characterisation of the orange pigment produced by a cold adapted strain of Penicillium sp. (GBPI_P155) isolated from mountain ecosystem. Mycology 9(2):81–92. Google Scholar
  96. Pärnänen K, Karkman A, Virta M, Eronen-Rasimus E, Kaartokallio H (2015) Discovery of bacterial polyhydroxyalkanoate synthase (PhaC)-encoding genes from seasonal Baltic Sea ice and cold estuarine waters. Extremophiles 19(1):197–206. Google Scholar
  97. Parrilli E, Tutino ML (2017) Heterologous protein expression in Pseudoalteromonas haloplanktis TAC125. In: M R (ed) Psychrophiles: from biodiversity to biotechnology, Second edition, vol 2. Springer, Cham, pp 513–525Google Scholar
  98. Perfumo A, Banat IM, Marchant R (2018) Going green and cold: biosurfactants from low-temperature environments to biotechnology applications. Trends Biotechnol 36(3):277–289. Google Scholar
  99. Piette F, D’Amico S, Mazzucchelli G, Danchin A, Leprince P, Feller G (2011) Life in the cold: a proteomic study of cold-repressed proteins in the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125. Appl Environ Microbiol 77(11):3881–3883. Google Scholar
  100. Pummer BG, Budke C, Augustin-Bauditz S, Niedermeier D, Felgitsch L, Kampf CJ, Huber RG, Liedl KR, Loerting T, Moschen T, Schauperl M, Tollinger M, Morris CE, Wex H, Grothe H, Poschl U, Koop T, Frohlich-Nowoisky J (2015) Ice nucleation by water-soluble macromolecules. Atmos Chem Phys 15(8):4077–4091. Google Scholar
  101. Raymond JA, Christner BC, Schuster SC (2008) A bacterial ice-binding protein from the Vostok ice core. Extremophiles 12(5):713–717. Google Scholar
  102. Raymond-Bouchard I, Goordial J, Zolotarov Y, Ronholm J, Stromvik M, Bakermans C, Whyte LG (2018) Conserved genomic and amino acid traits of cold adaptation in subzero-growing Arctic permafrost bacteria. FEMS Microbiol Ecol 94(4).
  103. Regand A, Goff HD (2006) Ice recrystallization inhibition in ice cream as affected by ice structuring proteins from winter wheat grass. J Dairy Sci 89(1):49–57. Google Scholar
  104. Rodrigues DF, Ivanova N, He Z, Huebner M, Zhou J, Tiedje JM (2008) Architecture of thermal adaptation in an Exiguobacterium sibiricum strain isolated from 3 million year old permafrost: a genome and transcriptome approach. BMC Genomics 9:547. Google Scholar
  105. Romero-Romero ML, Inglés-Prieto A, Ibarra-Molero B, Sanchez-Ruiz JM (2011) Highly anomalous energetics of protein cold denaturation linked to folding-unfolding kinetics. PLoS One 6(7):e23050–e23050. Google Scholar
  106. Roulling F, Godin A, Cipolla A, Collins T, Miyazaki K, Feller G (2016) Activity-stability relationships revisited in blue oxidases catalyzing electron transfer at extreme temperatures. Extremophiles 20(5):621–629. Google Scholar
  107. Russell NJ (1997) Psychrophilic bacteria—molecular adaptations of membrane lipids. Comp Biochem Physiol A Physiol 118:489–493Google Scholar
  108. Russell NJ (2008) Membrane components and cold sensing. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer Berlin Heidelberg, Berlin, pp 177–190Google Scholar
  109. Santiago M, Ramírez-Sarmiento CA, Zamora RA, Parra LP (2016) Discovery, molecular mechanisms, and industrial applications of cold-active enzymes. Front Microbiol 7(1408).
  110. Sarmiento F, Peralta R, Blamey JM (2015) Cold and hot extremozymes: industrial relevance and current trends. Front Bioeng Biotechnol 3:148. Google Scholar
  111. Shen L, Liu Y, Wang N, Jiao N, Xu B, Liu X (2018) Variation with depth of the abundance, diversity and pigmentation of culturable bacteria in a deep ice core from the Yuzhufeng Glacier, Tibetan Plateau. Extremophiles 22(1):29–38. Google Scholar
  112. Shulse CN, Allen EE (2011) Diversity and distribution of microbial long-chain fatty acid biosynthetic genes in the marine environment. Environ Microbiol 13(3):684–695. Google Scholar
  113. Siddiqui KS (2015) Some like it hot, some like it cold: temperature dependent biotechnological applications and improvements in extremophilic enzymes. Biotechnol Adv 33(8):1912–1922. Google Scholar
  114. Siddiqui KS, Williams TJ, Wilkins D, Yau S, Allen MA, Brown MV, Lauro FM, Cavicchioli R (2013) Psychrophiles. Annu Rev Earth Planet Sci 41(1):87–115. Google Scholar
  115. Singh AK, Sad K, Singh SK, Shivaji S (2014) Regulation of gene expression at low temperature: role of cold-inducible promoters. Microbiology 160(7):1291–1296. Google Scholar
  116. Singh A, Krishnan KP, Prabaharan D, Sinha RK (2017) Lipid membrane modulation and pigmentation: a cryoprotection mechanism in Arctic pigmented bacteria. J Basic Microbiol 57(9):770–780. Google Scholar
  117. Singh AK, Srivastava JK, Chandel AK, Sharma L, Mallick N, Singh SP (2019) Biomedical applications of microbially engineered polyhydroxyalkanoates: an insight into recent advances, bottlenecks, and solutions. Appl Microbiol Biotechnol.
  118. Soldatou S, Baker BJ (2017) Cold-water marine natural products, 2006 to 2016. Nat Prod Rep 34(6):585–626. Google Scholar
  119. Stritzler M, Diez Tissera A, Soto G, Ayub N (2018) Plant growth-promoting bacterium Pseudomonas fluorescens FR1 secrets a novel type of extracellular polyhydroxybutyrate polymerase involved in abiotic stress response in plants. Biotechnol Lett 40(9):1419–1423. Google Scholar
  120. Sun Y-Z, Yang H-L, Ma R-L, Zhang C-X, Lin W-Y (2011) Effect of dietary administration of Psychrobacter sp. on the growth, feed utilization, digestive enzymes and immune responses of grouper Epinephelus coioides. Aquac Nutr 17(3):e733–e740. Google Scholar
  121. Sweet CR, Watson RE, Landis CA, Smith JP (2015) Temperature-dependence of lipid A acyl structure in Psychrobacter cryohalolentis and Arctic isolates of Colwellia hornerae and Colwellia piezophila. Mar Drugs 13(8):4701–4720. Google Scholar
  122. Ting L, Williams TJ, Cowley MJ, Lauro FM, Guilhaus M, Raftery MJ, Cavicchioli R (2010) Cold adaptation in the marine bacterium, Sphingopyxis alaskensis, assessed using quantitative proteomics. Environ Microbiol 12(10):2658–2676. Google Scholar
  123. Tribelli PM, Lopez NI (2018) Reporting key features in cold-adapted bacteria. Life (Basel) 8(1).
  124. Tribelli PM, Solar Venero EC, Ricardi MM, Gómez-Lozano M, Raiger Iustman LJ, Molin S, López NI (2015) Novel essential role of ethanol oxidation genes at low temperature revealed by transcriptome analysis in the Antarctic bacterium Pseudomonas extremaustralis. PLoS One 10(12):e0145353. Google Scholar
  125. 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. Google Scholar
  126. Voets IK (2017) From ice-binding proteins to bio-inspired antifreeze materials. Soft Matter 13(28):4808–4823. Google Scholar
  127. Vollmers J, Voget S, Dietrich S, Gollnow K, Smits M, Meyer K, Brinkhoff T, Simon M, Daniel R (2013) Poles apart: Arctic and Antarctic Octadecabacter strains share high genome plasticity and a new type of xanthorhodopsin. PLoS One 8(5):e63422. Google Scholar
  128. Vollú RE, Jurelevicius D, Ramos LR, Peixoto RS, Rosado AS, Seldin L (2014) Aerobic endospore-forming bacteria isolated from Antarctic soils as producers of bioactive compounds of industrial interest. Polar Biol 37(8):1121–1131. Google Scholar
  129. Wani SH, Singh NB, Haribhushan A, Mir JI (2013) Compatible solute engineering in plants for abiotic stress tolerance—role of glycine betaine. Curr Genomics 14(3):157–165. Google Scholar
  130. Wanka KM, Damerau T, Costas B, Krueger A, Schulz C, Wuertz S (2018) Isolation and characterization of native probiotics for fish farming. BMC Microbiol 18(1):119–119. Google Scholar
  131. Yoshida K, Hashimoto M, Hori R, Adachi T, Okuyama H, Orikasa Y, Nagamine T, Shimizu S, Ueno A, Morita N (2016) Bacterial long-chain polyunsaturated fatty acids: their biosynthetic genes, functions, and practical use. Mar Drugs 14(5):94. Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Centre of Molecular and Environmental Biology (CBMA), Department of BiologyUniversity of MinhoBragaPortugal
  2. 2.Institute of MicrobiologyUniversity of InnsbruckInnsbruckAustria

Personalised recommendations