Skip to main content

Advertisement

Log in

Perspectives for using glacial and periglacial microorganisms for plant growth promotion at low temperatures

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Even though they are among the most extreme environments in which life can develop, glaciers are colonized by metabolically active microbes, some of which thrive—in their own particular way—under the prevailing harsh conditions. Glacial or periglacial microbes are often psychrophiles since they are able to grow optimally at low temperatures. This ability has evolved through a series of adaptations, both molecular and physiological, some of which have been exploited by the biotechnological industry to develop useful products and processes. The recent discovery of cold-adapted plant growth-promoting microorganisms (PGPM) in glacial ice or periglacial soils has opened a gate to a new trove of applications due to their potential use as biofertilizers or biocontrol agents, effective in cold climates. It has been claimed that this would be of profit to increase agriculture productivity in hilly terrains, like those prevailing in the Andes or the Himalayas, since—in addition to their ability to promote plant growth through direct or indirect mechanisms—they represent an environmentally friendly alternative to the use of pesticides and chemical fertilizers. In the following chapter, I summarize the current knowledge on the identity and characteristics of such PGPM and highlight the experiences in promoting the growth of a few plant species, at low temperatures.

Key Points

•Countless microbes are immured in glaciers and their surroundings.

•Many glacial and periglacial microbes are cold-loving (i.e., psychrophiles).

•Some glacial and periglacial psychrophiles promote plant growth and development.

•Plant growth-promoting psychrophiles can be used to develop biofertilizers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abyzov SS, Bobin NE, Koudryashov BB (1982) Quantitative assessment of microorganisms in microbiological studies of Antarctic glaciers. Biol Bull Acad Sci USSR 9:558–564

    Google Scholar 

  • Acuña-Rodríguez IS, Hansen H, Gallardo-Cerda J, Atala C, Molina-Montenegro MA (2019) Antarctic extremophiles: biotechnological alternative to crop productivity in saline soils. Front Bioeng Biotechnol 7:22. https://doi.org/10.3389/fbioe.2019.00022

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrews JH, Harris RF (2003) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180

    Article  Google Scholar 

  • Anesio AM, Lutz S, Chrismas NAM, Benning LG (2017) The microbiome of glaciers and ice sheets. NPJ Biofilms And Microbiomes 3:10. https://doi.org/10.1038/s41522-017-0019-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Balcazar W, Rondón J, Rengifo M, Ball M, Melfo A, Gómez W, Yarzábal LA (2015) Bioprospecting glacial ice for plant growth promoting bacteria. Microbiol Res 177:1–7. https://doi.org/10.1016/j.micres.2015.05.001

    Article  PubMed  Google Scholar 

  • Ball MM, Gómez W, Magallanes X, Moreno R, Melfo A, Yarzábal LA (2014) Bacteria recovered from a high-altitude, tropical glacier in Venezuelan Andes. World J Microbiol Biotechnol 30:931–941. https://doi.org/10.1007/s11274-013-1511-1

    Article  CAS  PubMed  Google Scholar 

  • Barroca M, Santos G, Gerday C, Collins T (2017) Biotechnological aspects of cold-active enzymes. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology. Springer, Cham, pp 461–475

    Chapter  Google Scholar 

  • Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A (2013) Characterization of a novel Antarctic plant growth- promoting bacterial strain and its interaction with Antarctic hair grass (Deschampsia antarctica Desv). Polar Biol 36:349–362

    Article  Google Scholar 

  • Bidle KD, Lee SH, Marchant DR, Falkowski PG (2007) Fossil genes and microbes in the oldest ice on earth. PNAS 104:13455–13460. https://doi.org/10.1073/pnas.0702196104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boetius A, Anesio AM, Deming JW, Mikucki JA, Rapp JZ (2015) Microbial ecology of the cryosphere: sea ice and glacial habitats. Nature Rev Microbiol 13:677–690

    Article  CAS  Google Scholar 

  • 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. Springer, Cham, pp 527–540

    Chapter  Google Scholar 

  • Bowman JP (2017) Genomics of psychrophilic bacteria and archaea. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology. Springer, Cham, pp 345–387

    Chapter  Google Scholar 

  • Boyd ES, Hamilton TL, Havig JR, Skidmore ML, Shock EL (2014) Chemolithotrophic primary production in a subglacial ecosystem. Appl Environ Microbiol 80:6146–6153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brouchkov A, Melnikov V, Kalenova L, Fursova O, Pogorelko G, Potapov V, Fursova N, Ignatov S, Brenner E, Bezrukov V, Muradian K (2017) Permafrost bacteria in biotechnology: biomedical applications. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology. Springer, Cham, pp 541–554

    Chapter  Google Scholar 

  • Buzzini P, Margesin R (2014) Cold-adapted yeasts: a lesson from the cold and a challenge for the XXI century. In: Buzzini P, Margesin R (eds) Cold-adapted yeasts. Springer, Berlin, pp 3–22. https://doi.org/10.1007/978-3-642-39681-6_1

    Chapter  Google Scholar 

  • Buzzini P, Branda E, Goretti M, Turchetti B (2012) Psychrophilic yeasts from worldwide glacial habitats: diversity, adaptation strategies and biotechnological potential. FEMS Microbiol Ecol 82:217–241

    Article  CAS  PubMed  Google Scholar 

  • Cavicchioli R, Charlton T, Ertan H, Mohd Omar S, Siddiqui KS, Williams TJ (2011) Biotechnological uses of enzymes from psychrophiles. Microb Biotechnol 4(4):449–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Zagorodnov V, Sandman K, Reeve JN (2000) Recovery and identification of viable bacteria immured in glacial ice. Icarus 144:479–485

    Article  Google Scholar 

  • Christner BC, Mosley-Thompson E, Thompson LG, Zagorodnov V, Sandman K, Reeve JN (2002) Isolation and identification of bacteria from ancient and modern ice core archives. In: Casassa G, Sepulveda FV, Sinclair R (eds) Patagonian ice fields. A unique natural laboratory for environmental and climate change studies. Kluwer, New York, pp 9–16

    Chapter  Google Scholar 

  • Christner BC, Royston-Bishop G, Foreman CM, Arnold BR, Tranter M, Welch KA, Lyons WB, Tsapin AI, Studinger M, Priscu J (2006) Limnological conditions in subglacial Lake Vostok, Antarctica. Limnol Oceanogr 51:2485–2501

    Article  Google Scholar 

  • Collins T, Gerday C (2017) Enzyme catalysis in Psychrophiles. In: Margesin R (ed) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 209–235. https://doi.org/10.1007/978-3-319-57057-0_10

    Chapter  Google Scholar 

  • Convey P, Gibson JA, Hillenbrand CD, Hodgson DA, Pugh PJ, Smellie JL, Stevens MI (2008) Antarctic terrestrial life–challenging the history of the frozen continent? Biol Rev 83:103–117. https://doi.org/10.1111/j.1469-185X.2008.00034.x

    Article  PubMed  Google Scholar 

  • D’Amico S, Collins T, Marx J-C, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7:385–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Elia T, Veerapaneni R, Rogers SO (2008) Isolation of microbes from Lake Vostok accretion ice. Appl Environ Microbiol 74(15):4962–4965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dimitrova D, Dorkov P, Gocheva B (2013) Antibiotic complex, produced by an Antarctic actinomycete strain Streptomyces anulatus 39 LBG09. Bulg J Agric Sci 19:72–76

    Google Scholar 

  • Edwards A (2015) Coming in from the cold: potential microbial threats from the terrestrial cryosphere. Front Earth Sci 3:12. https://doi.org/10.3389/feart.2015.00012

    Article  Google Scholar 

  • Encheva-Malinova M, Stoyanova M, Avramova H, Pavlova Y, Gocheva B, Ivanova I, Moncheva P (2014) Antibacterial potential of streptomycete strains from Antarctic soils. Biotechnol Biotechnol Equip 28(4):721–727. https://doi.org/10.1080/13102818.2014.947066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Encheva-Malinova M, Vancheva T, Badzhinerov N, Koleva V, Tishkov S, Bogatzevska N, Moncheva P (2015) Antimicrobial activity of Antarctic Streptomycetes against pepper bacterial spot causing agents. Annuaire de l’Université de Sofia “St Kliment Ohridski” Faculte de Biologie 100(4):216–222

    Google Scholar 

  • FAO (2017) The future of food and agriculture – trends and challenges. Rome. Available at: http://www.fao.org/3/a-i6583e.pdf

  • Fegel TS, Baron JS, Fountain AG, Johnson GF, Hall EK (2016) The differing biogeochemical and microbial signatures of glaciers and rock glaciers. J Geophys Res Biogeosci 121:919–932

    Article  CAS  Google Scholar 

  • Feller G (2013) Psychrophilic enzymes: from folding to function and biotechnology. Scientifica, Article ID 512840:28 pages. https://doi.org/10.1155/2013/512840

  • Feller G, Margesin R (2012) Polar microorganisms and biotechnology. In: Miller RV, Whyte LG (eds) Polar microbiology: life in a deep freeze. ASM Press, Washington, DC, pp 166–180

    Google Scholar 

  • Gallardo-Cerda J, Levihuan J, Lavín P, Oses R, Atala C, Torres-Díaz C, Cuba-Díaz M, Barrera A, Molina-Montenegro MA (2018) Antarctic rhizobacteria improve salt tolerance and physiological performance of the Antarctic vascular plants. Polar Biol 41:1973–1982. https://doi.org/10.1007/s00300-018-2336-z

    Article  Google Scholar 

  • Gesheva V (2010) Production of antibiotics and enzymes by soil microorganisms from the windmill islands region, Wilkes Land, East Antarctica. Polar Biol 33:1351–1357

    Article  Google Scholar 

  • Gidekel M, Gutiérrez A, Barrientos L, Cabrera G, Berríos G, Mihovilovic I (2010) Biofertilizer formulation. US patent application US 2010/0234222 A1

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica Article ID 963401, 15 p. https://doi.org/10.6064/2012/963401

  • Hamilton TL, Peters JW, Skidmore ML, Boyd ES (2013) Molecular evidence for an active endogenous microbiome beneath glacial ice. ISME J 7:1402–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hibbing M, Fuqua C, Parsek M, Brook Peterson S (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. https://doi.org/10.1038/nrmicro2259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Satler B (2008) Glacial ecosystems. Ecol Monogr 78:41–67

    Article  Google Scholar 

  • Hotaling S, Hood E, Hamilton TL (2017) Microbial ecology of mountain glacier ecosystems: biodiversity, ecological connections and implications of a warming climate. Environ Microbiol 19:2935–2948. https://doi.org/10.1111/1462-2920.13766

    Article  PubMed  Google Scholar 

  • Kalkreuter E, Pan G, Cepeda AJ, Shen B (2020) Targeting bacterial genomes for natural product discovery. Trends Pharmacol Sci 41:13–26

    Article  CAS  PubMed  Google Scholar 

  • Kloepper JW, Schroth MN (1981) Relationship of in vitro antibiosis of plant growth promoting rhizobacteria to plant growth and the displacement of root microflora. Phytopathology 71:1020–1024

    Article  Google Scholar 

  • Mahanty T, Bhattacharjee S, Goswami M, Bhattacharyya P, Das B, Ghosh A, Tribedi P (2017) Biofertilizers: a potential approach for sustainable agriculture development. Environ Sci Pollut Res 24:3315–3335. https://doi.org/10.1007/s11356-016-8104-0

    Article  CAS  Google Scholar 

  • Martínez-Rosales C, Fullana N, Musto H, Castro-Sowinski S (2012) Antarctic DNA moving forward: genomic plasticity and biotechnological potential. FEMS Microbiol Lett 331:1–9. https://doi.org/10.1111/j.1574-6968.2012.02531.x

    Article  CAS  PubMed  Google Scholar 

  • McLean AL (1918) Bacteria of ice and snow in Antarctica. Nature 102:35–39

    Article  Google Scholar 

  • Mieczen T, Gorniak D, Swiatecki A, Zdanowski M, Tarkowska-Kukuryk M, Adamczuk M (2013) Vertical microzonation of ciliates in cryoconite holes in ecology glacier, King George Island. Polish Polar Res 34:201–212

    Article  Google Scholar 

  • Miteva V (2008) Bacteria in snow and glacier ice. In: Margesin R, Schinner F, Marx JC, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 31–50

    Chapter  Google Scholar 

  • Motsara MR, Roy RN (2008) Guide to laboratory establishment for plant nutrient analysis. FAO Fertilizer and Plant Nutrition Bulletin 19 http://wwwfaoorg/3/i0131e/i0131e00htm Accessed 30 Dec 2019

  • Orellana-Saez M, Pacheco N, Costa JI, Mendez KN, Miossec MJ, Meneses C, Castro-Nallar E, Marcoleta AE, Poblete-Castro I (2019) In-depth genomic and phenotypic characterization of the Antarctic psychrotolerant strain Pseudomonas sp. MPC6 reveals unique metabolic features, plasticity, and biotechnological potential. Front Microbiol 10:1154. https://doi.org/10.3389/fmicb.2019.01154

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandey A, Yarzábal LA (2018) Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl Microbiol Biotechnol 103(2):643–657. https://doi.org/10.1007/s00253-018-9515-2

    Article  CAS  PubMed  Google Scholar 

  • Pandey A, Sharma E, Palni LMS (1998) Influence of bacterial inoculation on maize in upland farming systems of the Sikkim Himalaya. Soil Biol Biochem 30:379–384

    Article  CAS  Google Scholar 

  • Pingali PL (2012) Green revolution: impacts, limits, and the path ahead. Proc Natl Acad Sci U S A 109:3112302–3112308

    Article  Google Scholar 

  • Price PB (2000) A habitat for psychrophiles in deep Antarctic ice. Proc Natl Acad Sci U S A 97:1247–1251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price PB (2007) Microbial life in glacial ice and implications for a cold origin of life. FEMS Microbiol Ecol 59:217–231

    Article  CAS  PubMed  Google Scholar 

  • Priscu J, Christner B (2004) Earth's icy biosphere. In: Bull A (ed) Microbial diversity and bioprospecting. ASM Press, Washington DC, pp 130–145. https://doi.org/10.1128/9781555817770.ch13

    Chapter  Google Scholar 

  • Priscu JC, Christner BC, Foreman CM, Royston-Bishop G (2007) Biological material in ice cores. Encyclopedia of Quaternary Sciences. Elsevier, In

    Google Scholar 

  • Rahman S (2015) Green revolution in India: environmental degradation and impact on livestock. Asian J Water Environ Pollut 12:75–80

    Article  CAS  Google Scholar 

  • Ramos P, Rivas N, Pollmann S, Casati P, Molina-Montenegro MA (2018) Hormonal and physiological changes driven by fungal endophytes increase Antarctic plant performance under UV-B radiation. Fungal Ecol 34:76–82. https://doi.org/10.1016/j.funeco.2018.05.006

    Article  Google Scholar 

  • Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodríguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6(7):e14823. https://doi.org/10.1371/journal.pone.0014823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Research and Markets Report (2019) Biofertilizers market by form (Liquid, Carrier-Based), mode of application (Soil Treatment, Seed Treatment), crop type, type (Nitrogen-Fixing, Phosphate Solubilizing & Mobilizing, Potash Solubilizing & Mobilizing), Region - Global Forecast to 2025. Available at: https://www.researchandmarkets.com/reports/4833505/biofertilizers-market-by-form-liquid-carrier?utm_source=dynamic&utm_medium=GNOM&utm_code=tqnt96&utm_campaign=1320628+-+World+Biofertilizers+Market+Report+2019-2025%3a+%243.8B+Opportunity+Outlook+with+an+Overview+of+the+Competitive+Landscape&utm_exec=joca220gnomd

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogers SO, Starmer WT, Castello JD (2004) Recycling of pathogenic microbes through survival in ice. Med Hypotheses 63(5):773–777

    Article  PubMed  Google Scholar 

  • Rondón J, Gómez W, Ball MM, Melfo A, Rengifo M, Balcázar W, Dávila-Vera D, Balza-Quintero A, Mendoza-Briceño RV, Yarzábal LA (2016) Diversity of culturable bacteria recovered from Pico Bolívar’s glacial and subglacial environments, at 4950 m, in Venezuelan tropical Andes. Can J Microbiol 62:1–14. https://doi.org/10.1139/cjm-2016-0172

    Article  CAS  Google Scholar 

  • Rondón JJ, Ball MM, Castro LT, Yarzábal LA (2019) Eurypsychrophilic Pseudomonas spp. isolated from Venezuelan tropical glaciers as promoters of wheat growth and biocontrol agents of plant pathogens at low temperatures. Environ Sustain 2:265–275. https://doi.org/10.1007/s42398-019-00072-2

    Article  CAS  Google Scholar 

  • Scott R, Theraisnathan V, Ma L-J, Zhao Y, Zhang G, Shin S-G, Castello J, Starmer W (2004) Comparisons of protocols for decontamination of environmental ice samples for biological and molecular examinations. Appl Environ Microbiol 70:2540–2544. https://doi.org/10.1128/AEM.70.4.2540-2544.2004

    Article  CAS  Google Scholar 

  • Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer Plus 2:587 http://www.springerplus.com/content/2/1/587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22(2):123–131

    Article  CAS  PubMed  Google Scholar 

  • Skidmore M, Anderson SP, Sharp M, Foght J, Lanoil BD (2005) Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl Environ Microbiol 71:6986–6997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tapia Vázquez I, Sánchez R, Arroyo M, Lira-Ruan V, Sánchez-Reyes A, Sánchez-Carbente MR, Padilla-Chacón D, Batista-García RA, Folch-Mallol JL (2020) Isolation and characterization of psychrophilic and psychrotolerant plant-growth promoting microorganisms from a high-altitude volcano crater in Mexico. Microbial Res 232:126394. https://doi.org/10.1016/j.micres.2019.126294

  • Toubes-Rodrigo M, Cook SJ, Elliot D, Sen R (2016) Sampling and describing glacier ice. In: Cook SJ, Clarke L, Nield J (eds) Geomorphological Techniques. Chap. 3, Sec. 4.1. British Society for Geomorphology, London, pp 1–9

    Google Scholar 

  • Tung HC, Bramall NE, Price BP (2005) Microbial origin of excess methane in glacial ice and implications for life on Mars. Proc Natl Acad Sci USA (PNAS) 102:18292–18296

    Article  CAS  Google Scholar 

  • Turner BL, Frossard E, Oberson A (2006) Enhancing phosphorus availability in low-fertility soils. In: Uphoff NT et al (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton, pp 191–205

    Chapter  Google Scholar 

  • U.S. Geological Survey (n.d.). What is a glacier? Available at: https://www.usgs.gov/faqs/what-a-glacier?qt-news_science_products=0#qt-news_science_products

  • Weil T, De Filippo C, Albanese D, Donati C, Pindo M, Pavarini L, Carotenuto F, Pasqui M, Poto L, Gabrieli J, Barbante C, Sattler B, Cavalieri D, Miglietta F (2017) Legal immigrants: invasion of alien microbial communities during winter occurring desert dust storms. Microbiome 5:32. https://doi.org/10.1186/s40168-017-0249-7

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K (2013) Microbial biodiversity in glacier-fed streams. ISME J 7:1651–1660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yarzábal LA (2014) Cold-tolerant phosphate solubilizing microorganisms and agriculture development in mountainous regions of the world. In: Saghir Khan M et al (eds) Phosphate solubilizing microorganisms. Principles and applications of Microphos technology. Springer International Publishing, Cham, pp 113–135. https://doi.org/10.1007/978-3-319-08216-5_5

    Chapter  Google Scholar 

  • Yarzábal LA, Chica E (2017) Potential for developing low-input sustainable agriculture in the tropical Andes by making use of native microbial resources. In: Singh D, Singh H, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives, Microbial interactions and agro-ecological impacts, vol 2. Springer, Singapore, pp 29–54

    Google Scholar 

  • Yarzábal LA, Monserrate M, Buela L, Chica E (2018) Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biology 41(11):2343–2354. https://doi.org/10.1007/s00300-018-2374-6

    Article  Google Scholar 

  • Zemp M, Huss M, Thibert E, Eckert N, McNabb R, Huber J, Barandun M, Machguth H, Nussbaumer SU, Gärtner-Roer I, Thomson L, Paul F, Maussion F, Kutuzov S, Cogley JG (2019) Global glacier mass changes and their contributions to sea-level rise from 1961 to 2016. Nature 568:382–386. https://doi.org/10.1038/s41586-019-1071-0

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Dr. Eduardo Chica (Facultad de Ciencias Agropecuarias, Universidad de Cuenca, Ecuador) is gratefully acknowledged for critical reading and editing of the original manuscript.

Author information

Authors and Affiliations

Authors

Contributions

LAY conceived the present review, performed the bibliographic research, and wrote the manuscript.

Corresponding author

Correspondence to Luis Andrés Yarzábal.

Ethics declarations

Conflict of interest

The author declares that he has no competing interests.

Human and animal rights and informed consent

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

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yarzábal, L.A. Perspectives for using glacial and periglacial microorganisms for plant growth promotion at low temperatures. Appl Microbiol Biotechnol 104, 3267–3278 (2020). https://doi.org/10.1007/s00253-020-10468-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10468-4

Keywords

Navigation