Biology:Psychrophile

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Short description: Organism capable of growing and reproducing in the cold
The lichen Xanthoria elegans can continue to photosynthesize at −24 °C.[1]

Psychrophiles or cryophiles (adj. psychrophilic or cryophilic) are extremophilic organisms that are capable of growth and reproduction in low temperatures, ranging from −20 °C (−4 °F)[2] to 20 °C (68 °F).[3] They are found in places that are permanently cold, such as the polar regions and the deep sea. They can be contrasted with thermophiles, which are organisms that thrive at unusually high temperatures, and mesophiles at intermediate temperatures. Psychrophile is Greek for 'cold-loving', from grc ψυχρός (psukhrós) 'cold, frozen'.

Many such organisms are bacteria or archaea, but some eukaryotes such as lichens, snow algae, phytoplankton, fungi, and wingless midges, are also classified as psychrophiles.

Biology

Snow surface with snow algae Chlamydomonas nivalis.

Habitat

The cold environments that psychrophiles inhabit are ubiquitous on Earth, as a large fraction of the planetary surface experiences temperatures lower than 10 °C. They are present in permafrost, polar ice, glaciers, snowfields and deep ocean waters. These organisms can also be found in pockets of sea ice with high salinity content.[4] Microbial activity has been measured in soils frozen below −39 °C.[5] In addition to their temperature limit, psychrophiles must also adapt to other extreme environmental constraints that may arise as a result of their habitat. These constraints include high pressure in the deep sea, and high salt concentration on some sea ice.[6][4]

Adaptations

Psychrophiles are protected from freezing and the expansion of ice by ice-induced desiccation and vitrification (glass transition), as long as they cool slowly. Free living cells desiccate and vitrify between −10 °C and −26 °C. Cells of multicellular organisms may vitrify at temperatures below −50 °C. The cells may continue to have some metabolic activity in the extracellular fluid down to these temperatures, and they remain viable once restored to normal temperatures.[2]

They must also overcome the stiffening of their lipid cell membrane, as this is important for the survival and functionality of these organisms. To accomplish this, psychrophiles adapt lipid membrane structures that have a high content of short, unsaturated fatty acids. Compared to longer saturated fatty acids, incorporating this type of fatty acid allows for the lipid cell membrane to have a lower melting point, which increases the fluidity of the membranes.[7][8] In addition, carotenoids are present in the membrane, which help modulate the fluidity of it.[9]

Antifreeze proteins are also synthesized to keep psychrophiles' internal space liquid, and to protect their DNA when temperatures drop below water's freezing point. By doing so, the protein prevents any ice formation or recrystallization process from occurring.[9]

The enzymes of these organisms have been hypothesized to engage in an activity-stability-flexibility relationship as a method for adapting to the cold; the flexibility of their enzyme structure will increase as a way to compensate for the freezing effect of their environment.[4]

Certain cryophiles, such as Gram-negative bacteria Vibrio and Aeromonas spp., can transition into a viable but nonculturable (VBNC) state.[10] During VBNC, a micro-organism can respire and use substrates for metabolism – however, it cannot replicate. An advantage of this state is that it is highly reversible. It has been debated whether VBNC is an active survival strategy or if eventually the organism's cells will no longer be able to be revived.[11] There is proof however it may be very effective – Gram positive bacteria Actinobacteria have been shown to have lived about 500,000 years in the permafrost conditions of Antarctica, Canada, and Siberia.[12]

Taxonomic range

Psychrophiles include bacteria, lichens, snow algae, phytoplankton, fungi, and insects.

Among the bacteria that can tolerate extreme cold are Arthrobacter sp., Psychrobacter sp. and members of the genera Halomonas, Pseudomonas, Hyphomonas, and Sphingomonas.[13] Another example is Chryseobacterium greenlandensis, a psychrophile that was found in 120,000-year-old ice.

Umbilicaria antarctica and Xanthoria elegans are lichens that have been recorded photosynthesizing at temperatures ranging down to −24 °C, and they can grow down to around −10 °C.[14][1] Some multicellular eukaryotes can also be metabolically active at sub-zero temperatures, such as some conifers;[15] those in the Chironomidae family are still active at −16 °C.[16]

Psychrophilic algae can tolerate cold temperatures, like this Chlamydomonas green algae growing on snow in Antarctica.

Microalgae that live in snow and ice include green, brown, and red algae. Snow algae species such as Chloromonas sp., Chlamydomonas sp., and Chlorella sp. are found in polar environments.[17][18]

Some phytoplankton can tolerate extremely cold temperatures and high salinities that occur in brine channels when sea ice forms in polar oceans. Some examples are diatoms like Fragilariopsis cylindrus, Nitzchia lecointeii, Entomoneis kjellmanii, Nitzchia stellata, Thalassiosira australis, Berkelaya adeliense, and Navicula glaciei.[19][20][21]

Penicillium is a genus of fungi found in a wide range of environments including extreme cold.[22]

Among the psychrophile insects, the Grylloblattidae or ice crawlers, found on mountaintops, have optimal temperatures between 1–4 °C.[23] The wingless midge (Chironomidae) Belgica antarctica can tolerate salt, being frozen and strong ultraviolet, and has the smallest known genome of any insect. The small genome, of 99 million base pairs, is thought to be adaptive to extreme environments.[24]

Psychrotrophic bacteria

Psychrotrophic microbes are able to grow at temperatures below 7 °C (44.6 °F), but have better growth rates at higher temperatures. Psychrotrophic bacteria and fungi are able to grow at refrigeration temperatures, and can be responsible for food spoilage and as foodborne pathogens such as Yersinia. They provide an estimation of the product's shelf life, but also they can be found in soils,[25] in surface and deep sea waters,[26] in Antarctic ecosystems,[27] and in foods.[28]

Psychrotrophic bacteria are of particular concern to the dairy industry.[29][self-published source?] Most are killed by pasteurization; however, they can be present in milk as post-pasteurization contaminants due to less than adequate sanitation practices. According to the Food Science Department at Cornell University, psychrotrophs are bacteria capable of growth at temperatures at or less than 7 °C (44.6 °F). At freezing temperatures, growth of psychrotrophic bacteria becomes negligible or virtually stops.[30]

All three subunits of the RecBCD enzyme are essential for physiological activities of the enzyme in the Antarctic Pseudomonas syringae, namely, repairing of DNA damage and supporting the growth at low temperature. The RecBCD enzymes are exchangeable between the psychrophilic P. syringae and the mesophilic E. coli when provided with the entire protein complex from same species. However, the RecBC proteins (RecBCPs and RecBCEc) of the two bacteria are not equivalent; the RecBCEc is proficient in DNA recombination and repair, and supports the growth of P. syringae at low temperature, while RecBCPs is insufficient for these functions. Finally, both helicase and nuclease activity of the RecBCDPs are although important for DNA repair and growth of P. syringae at low temperature, the RecB-nuclease activity is not essential in vivo.[31]

Psychrophilic microalgae

Antarctic diatom algae covering the underwater surface of broken sea ice in the Ross Sea.

Microscopic algae that can tolerate extremely cold temperatures can survive in snow, ice, and very cold seawater. On snow, cold-tolerant algae can bloom on the snow surface covering land, glaciers, or sea ice when there is sufficient light. These snow algae darken the surface of the snow and can contribute to snow melt.[18] In seawater, phytoplankton that can tolerate both very high salinities and very cold temperatures are able to live in sea ice. One example of a psychrophilic phytoplankton species is the ice-associated diatom Fragilariopsis cylindrus.[19] Phytoplankton living in the cold ocean waters near Antarctica often have very high protein content, containing some of the highest concentrations ever measured of enzymes like Rubisco.[20]

Psychrotrophic insects

The wingless midge (Chironomidae) Belgica antarctica.

Insects that are psychrotrophic can survive cold temperatures through several general mechanisms (unlike opportunistic and chill susceptible insects): (1) chill tolerance, (2) freeze avoidance, and (3) freeze tolerance.[32] Chill tolerant insects succumb to freezing temperatures after prolonged exposure to mild or moderate freezing temperatures.[33] Freeze avoiding insects can survive extended periods of time at sub-freezing temperatures in a supercooled state, but die at their supercooling point.[33] Freeze tolerant insects can survive ice crystal formation within their body at sub-freezing temperatures.[33] Freeze tolerance within insects is argued to be on a continuum, with some insect species exhibiting partial (e.g., Tipula paludosa,[34] Hemideina thoracica[35] ), moderate (e.g., Cryptocercus punctulatus[36]), and strong freezing tolerance (e.g., Eurosta solidaginis[37] and Syrphus ribesii[38]), and other insect species exhibiting freezing tolerance with low supercooling point (e.g., Pytho deplanatus[39]).[32]

Psychrophile versus psychrotroph

In 1940, ZoBell and Conn stated that they had never encountered "true psychrophiles" or organisms that grow best at relatively low temperatures.[40] In 1958, J. L. Ingraham supported this by concluding that there are very few or possibly no bacteria that fit the textbook definitions of psychrophiles. Richard Y. Morita emphasizes this by using the term psychrotroph to describe organisms that do not meet the definition of psychrophiles. The confusion between the terms psychrotrophs and psychrophiles was started because investigators were unaware of the thermolability of psychrophilic organisms at the laboratory temperatures. Due to this, early investigators did not determine the cardinal temperatures for their isolates.[41]

The similarity between these two is that they are both capable of growing at zero, but optimum and upper temperature limits for the growth are lower for psychrophiles compared to psychrotrophs.[42] Psychrophiles are also more often isolated from permanently cold habitats compared to psychrotrophs. Although psychrophilic enzymes remain under-used because the cost of production and processing at low temperatures is higher than for the commercial enzymes that are presently in use, the attention and resurgence of research interest in psychrophiles and psychrotrophs will be a contributor to the betterment of the environment and the desire to conserve energy.[42]

See also

References

  1. ↑ 1.0 1.1 Barták, Miloš; Váczi, Peter; Hájek, Josef; Smykla, Jerzy (2007). "Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans". Polar Biology 31 (1): 47–51. doi:10.1007/s00300-007-0331-x. 
  2. ↑ 2.0 2.1 Neufeld, Josh; Clarke, Andrew; Morris, G. John; Fonseca, Fernanda; Murray, Benjamin J.; Acton, Elizabeth; Price, Hannah C. (2013). "A Low Temperature Limit for Life on Earth". PLOS One 8 (6): e66207. doi:10.1371/journal.pone.0066207. PMID 23840425. Bibcode: 2013PLoSO...866207C. 
  3. ↑ Moyer, Craig L.; Collins, Eric R.; Morita, Richard Y. (2017-01-01). "Psychrophiles and Psychrotrophs" (in en). Reference Module in Life Sciences (Elsevier). doi:10.1016/b978-0-12-809633-8.02282-2. ISBN 978-0-12-809633-8. https://www.sciencedirect.com/science/article/pii/B9780128096338022822. Retrieved 2022-05-22. 
  4. ↑ 4.0 4.1 4.2 D'Amico, Salvino; Tony Collins; Jean-Claude Marx; Georges Feller; Charles Gerday (2006). "Psychrophilic Microorganisms: Challenges for Life". EMBO Reports 7 (4): 385–9. doi:10.1038/sj.embor.7400662. PMID 16585939. 
  5. ↑ Panikov, N.S.; Flanagan, P.W.; Oechel, W.C.; Mastepanov, M.A.; Christensen, T.R. (2006). "Microbial activity in soils frozen to below −39°C". Soil Biology and Biochemistry 38 (4): 785–794. doi:10.1016/j.soilbio.2005.07.004. 
  6. ↑ Feller, Georges; Gerday, Charles (December 2003). "Psychrophilic enzymes: hot topics in cold adaptation". Nature Reviews Microbiology 1 (3): 200–208. doi:10.1038/nrmicro773. PMID 15035024. 
  7. ↑ Chattopadhyay, M. K.; Jagannadham, M. V. (2003). "A branched chain fatty acid promotes cold adaptation in bacteria". Journal of Biosciences 28 (4): 363–364. doi:10.1007/bf02705110. PMID 12799482. 
  8. ↑ Erimban, S.; Daschakraborty, S. (2020). "Cryostabilization of the Cell Membrane of a Psychrotolerant Bacteria via Homeoviscous Adaptation". J. Phys. Chem. Lett. 11 (18): 7709–7716. doi:10.1021/acs.jpclett.0c01675. PMID 32840376. 
  9. ↑ 9.0 9.1 Chattopadhyay, M. K. (2006). "Mechanism of bacterial adaptation to low temperature". Journal of Biosciences 31 (1): 157–165. doi:10.1007/bf02705244. PMID 16595884. 
  10. ↑ Maayer, Pieter De; Anderson, Dominique; Cary, Craig; Cowan, Don A. (May 15, 2015). "Some like it cold: understanding the survival strategies of psychrophiles". EMBO Reports 15 (5): 508–517. doi:10.1002/embr.201338170. PMID 24671034. 
  11. ↑ Li, Laam; Mendis, Nilmini; Trigui, Hana; Oliver, James D.; Faucher, Sebastien P. (2014). "The importance of the viable but non-culturable state in human bacterial pathogens". Frontiers in Microbiology 5: 258. doi:10.3389/fmicb.2014.00258. PMID 24917854. 
  12. ↑ Johnson, Sarah Stewart; Hebsgaard, Martin B.; Christensen, Torben R.; Mastepanov, Mikhail; Nielsen, Rasmus; Munch, Kasper; Brand, Tina; Gilbert, M. Thomas P. et al. (2007). "Ancient bacteria show evidence of DNA repair". Proceedings of the National Academy of Sciences 104 (36): 14401–5. doi:10.1073/pnas.0706787104. PMID 17728401. Bibcode: 2007PNAS..10414401J. 
  13. ↑ Siddiqui, Khawar S.; Williams, Timothy J.; Wilkins, David; Yau, Sheree; Allen, Michelle A.; Brown, Mark V.; Lauro, Federico M.; Cavicchioli, Ricardo (2013). "Psychrophiles". Annual Review of Earth and Planetary Sciences 41: 87–115. doi:10.1146/annurev-earth-040610-133514. Bibcode: 2013AREPS..41...87S. 
  14. ↑ Clarke, Andrew (2014). "The thermal limits to life on Earth". International Journal of Astrobiology 13 (2): 141–154. doi:10.1017/S1473550413000438. Bibcode: 2014IJAsB..13..141C. http://nora.nerc.ac.uk/id/eprint/507274/1/Clarke.pdf. 
  15. ↑ Riou-Nivert, Philippe (2001). Les résineux - Tome 1 : connaissance et reconnaissance. Institut pour le développement forestier. p. 79. 
  16. ↑ Kohshima, Shiro (1984). "A novel cold-tolerant insect found in a Himalayan glacier". Nature 310 (5974): 225–227. doi:10.1038/310225a0. Bibcode: 1984Natur.310..225K. 
  17. ↑ Davey, Matthew P.; Norman, Louisa; Sterk, Peter; Huete‐Ortega, Maria; Bunbury, Freddy; Loh, Bradford Kin Wai; Stockton, Sian; Peck, Lloyd S. et al. (27 February 2019). "Snow algae communities in Antarctica: metabolic and taxonomic composition". New Phytologist (Wiley) 222 (3): 1242–1255. doi:10.1111/nph.15701. ISSN 0028-646X. PMID 30667072. 
  18. ↑ 18.0 18.1 Khan, Alia L.; Dierssen, Heidi M.; Scambos, Ted A.; Höfer, Juan; Cordero, Raul R. (13 January 2021). "Spectral characterization, radiative forcing and pigment content of coastal Antarctic snow algae: approaches to spectrally discriminate red and green communities and their impact on snowmelt". The Cryosphere (Copernicus GmbH) 15 (1): 133–148. doi:10.5194/tc-15-133-2021. ISSN 1994-0424. Bibcode: 2021TCry...15..133K. 
  19. ↑ 19.0 19.1 Lauritano, Chiara; Rizzo, Carmen; Lo Giudice, Angelina; Saggiomo, Maria (9 December 2020). "Physiological and Molecular Responses to Main Environmental Stressors of Microalgae and Bacteria in Polar Marine Environments". Microorganisms (MDPI AG) 8 (12): 1957. doi:10.3390/microorganisms8121957. ISSN 2076-2607. PMID 33317109. 
  20. ↑ 20.0 20.1 Young, Jodi N.; Goldman, Johanna A. L.; Kranz, Sven A.; Tortell, Philippe D.; Morel, Francois M. M. (3 October 2014). "Slow carboxylation of R ubisco constrains the rate of carbon fixation during A ntarctic phytoplankton blooms". New Phytologist (Wiley) 205 (1): 172–181. doi:10.1111/nph.13021. ISSN 0028-646X. PMID 25283055. 
  21. ↑ Young, JN; Kranz, SA; Goldman, JAL; Tortell, PD; Morel, FMM (21 July 2015). "Antarctic phytoplankton down-regulate their carbon-concentrating mechanisms under high CO2 with no change in growth rates". Marine Ecology Progress Series (Inter-Research Science Center) 532: 13–28. doi:10.3354/meps11336. ISSN 0171-8630. Bibcode: 2015MEPS..532...13Y. 
  22. ↑ Gupta, G.N.; Srivastava, S.; Khare, S.K.; Prakash, V. (2014). "Extremophiles: An Overview of Microorganism from Extreme Environment". International Journal of Agriculture, Environment and Biotechnology 7 (2): 371. doi:10.5958/2230-732x.2014.00258.7. 
  23. ↑ Grimaldi, David; Engel, Michael S. (2005). "Polyneoptera: Grylloblattodea: The Ice Crawlers". Evolution of the Insects. New York City: Cambridge University Press. pp. 222–224. ISBN 9780521821490. 
  24. ↑ Gough, Zoe (12 August 2014). "Antarctic midge has smallest insect genome". BBC. https://www.bbc.co.uk/nature/28525963. 
  25. ↑ Druce, R. G.; Thomas, S. B. (1970). "An Ecological Study of the Psychrotrophic Bacteria of Soil, Water, Grass and Hay". Journal of Applied Bacteriology 33 (2): 420–435. doi:10.1111/j.1365-2672.1970.tb02215.x. PMID 5448255. 
  26. ↑ Radjasa, Ocky Karna; Urakawa, Hidetoshi; Kita-Tsukamoto, Kumiko; Ohwada, Kouichi (2001). "Characterization of Psychrotrophic Bacteria in the Surface and Deep-Sea Waters from the Northwestern Pacific Ocean Based on 16S Ribosomal DNA Analysis". Marine Biotechnology 3 (5): 454–462. doi:10.1007/s10126-001-0050-1. PMID 14961338. http://eprints.undip.ac.id/355/1/Abstract_of_01OckyMarBiotech-2001.PDF. 
  27. ↑ Correa-Guimaraes, A.; Martín-Gil, J.; Ramos-Sánchez, M. C.; Vallejo-Pérez, L. (2007). "Psychrotrophic bacteria isolated from Antarctic ecosystems". Department of Forestry, Agricultural and Environmental Engineering, ETSIA, Avenida de Madrid, 57, Palencia, Spain. http://es.scribd.com/doc/33323896/Psychrotrophic-Bacteria. 
  28. ↑ "Psychrotrophic Bacteria in Foods: Disease and Spoilage. – Food Trade Review". Encyclopedia.com. 1993-09-01. http://www.encyclopedia.com/doc/1G1-14605181.html. 
  29. ↑ "The case of Psychrotrophic bacteria". Leon the Milkman's Blog. 2006-03-18. http://www.leonthemilkman.com/2006/03/18/the-case-of-psychrotrophic-bacteria/. 
  30. ↑ Steven C. Murphy, "Shelf Life of Fluid Milk Products – Microbial Spoilage", Food Science Department, Cornell University.. Retrieved 22 November 2009.
  31. ↑ Pavankumar, Theetha L.; Sinha, Anurag K.; Ray, Malay K. (2010). "All Three Subunits of RecBCD Enzyme Are Essential for DNA Repair and Low-Temperature Growth in the Antarctic Pseudomonas syringae Lz4W". PLOS ONE 5 (2): e9412. doi:10.1371/journal.pone.0009412. PMID 20195537. Bibcode: 2010PLoSO...5.9412P. 
  32. ↑ 32.0 32.1 Sinclair, B. (1999). "Insect cold tolerance: How many kinds of frozen?". Eur. J. Entomol. 96: 157–164. https://www.eje.cz/artkey/eje-199902-0009_Insect_cold_tolerance_How_many_kinds_of_frozen.php. 
  33. ↑ 33.0 33.1 33.2 Bale, J. (1996). "Insect cold hardiness: A matter of life and death". Eur. J. Entomol. 93: 369–382. https://www.eje.cz/artkey/eje-199603-0009_Insect_cold_hardiness_A_matter_of_life_and_death.php. 
  34. ↑ Todd, C.; Block, W. (1995). "A comparison of the cold hardiness attributes in larvae of four species of Diptera". CryoLetters 16: 137–146. 
  35. ↑ Sinclair, Brent J.; Worland, M. Roger; Wharton, David A. (March 1999). "Ice nucleation and freezing tolerance in New Zealand alpine and lowland weta, Hemideina spp. (Orthoptera: Stenopelmatidae)". Physiological Entomology 24 (1): 56–63. doi:10.1046/j.1365-3032.1999.00112.x. ISSN 0307-6962. 
  36. ↑ Hamilton, R. L.; Mullins, D. E.; Orcutt, D. M. (1985). "Freezing-tolerance in the woodroachCryptocercus punctulatus (Scudder)". Experientia 41 (12): 1535–1537. doi:10.1007/BF01964793. ISSN 0014-4754. 
  37. ↑ Baust, John G.; Nishino, Misako (1991). "Freezing Tolerance in the Goldenrod Gall Fly (Eurosta solidaginis)". Insects at Low Temperature. pp. 260–275. doi:10.1007/978-1-4757-0190-6_11. ISBN 978-1-4757-0192-0. 
  38. ↑ Hart, Andrew; Bale, Jeffrey (1997). "Evidence for the first strongly freeze-tolerant insect found in the U.K.". Ecological Entomology 22 (2): 242–245. doi:10.1046/j.1365-2311.1997.t01-1-00048.x. ISSN 0307-6946. 
  39. ↑ Ring, Richard A (1982). "Freezing-tolerant insects with low supercooling points". Comparative Biochemistry and Physiology Part A: Physiology 73 (4): 605–612. doi:10.1016/0300-9629(82)90267-5. ISSN 0300-9629. 
  40. ↑ Ingraham, J. L. (1958). "Growth of psychrophilic bacteria". Journal of Bacteriology 76 (1): 75–80. doi:10.1128/jb.76.1.75-80.1958. PMID 13563393. 
  41. ↑ Morita, Richard Y. (1975). "Psychrophilic bacteria". Bacteriological Reviews 39 (2): 144–67. doi:10.1128/br.39.2.144-167.1975. PMID 1095004. 
  42. ↑ 42.0 42.1 "Cold Adaptation of Microorganisms [and Discussion]". Philosophical Transactions of the Royal Society of London. Series B Biological Sciences 326 (1237, Life at Low Temperatures): 595–611. 1990. doi:10.1098/rstb.1990.0034. PMID 1969649. Bibcode: 1990RSPTB.326..595R. 

Further reading

  • Bej, Asim K.; Jackie Aislabie; Ronald M. Atlas (15 December 2009). Polar Microbiology: The Ecology, Biodiversity and Bioremediation Potential of Microorganisms in Extremely Cold Environments. Crc Pr Inc. ISBN 978-1420083842. 
  • Murata, Yoshinori (2006). "Genome-wide expression analysis of yeast response during exposure to 4C". Extremophiles 10 (2): 117–128. doi:10.1007/s00792-005-0480-1. PMID 16254683. 
  • Mikucki, J. A. (2009). "A contemporary microbially maintained subglacial ferrous 'ocean'". Science 324 (5925): 397–400. doi:10.1126/science.1167350. PMID 19372431. Bibcode: 2009Sci...324..397M. 
  • Sandle, T.; Skinner, K. (2013). "Study of psychrophilic and psychrotolerant microorganisms isolated in cold rooms used for pharmaceutical processing". Journal of Applied Microbiology 114 (4): 1166–1174. doi:10.1111/jam.12101. PMID 23216715. 



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