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Diverse microbial species survive high ammonia concentrations

Published online by Cambridge University Press:  03 February 2012

Laura C. Kelly ,
Charles S. Cockell  and
Stephen Summers
Laura C. Kelly*
Affiliation:
Geomicrobiology Research Group, CEPSAR, Open University, Milton Keynes MK7 6AA, UK
Charles S. Cockell
Affiliation:
Geomicrobiology Research Group, CEPSAR, Open University, Milton Keynes MK7 6AA, UK School of Physics and Astronomy, James Clerk Maxwell Building, The Kings Building, University of Edinburgh, Edinburgh EH9 2JZ, UK
Stephen Summers
Affiliation:
Geomicrobiology Research Group, CEPSAR, Open University, Milton Keynes MK7 6AA, UK Molecular Microbial Ecology Laboratory, Centre for Ecology and Hydrology, Crowmarsh Gifford, Oxfordshire OX10 8BB, UK
*
e-mail: [email protected]
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Abstract

Planetary protection regulations are in place to control the contamination of planets and moons with terrestrial micro-organisms in order to avoid jeopardizing future scientific investigations relating to the search for life. One environmental chemical factor of relevance in extraterrestrial environments, specifically in the moons of the outer solar system, is ammonia (NH3). Ammonia is known to be highly toxic to micro-organisms and may disrupt proton motive force, interfere with cellular redox reactions or cause an increase of cell pH. To test the survival potential of terrestrial micro-organisms exposed to such cold, ammonia-rich environments, and to judge whether current planetary protection regulations are sufficient, soil samples were exposed to concentrations of NH3 from 5 to 35% (v/v) at −80°C and room temperature for periods up to 11 months. Following exposure to 35% NH3, diverse spore-forming taxa survived, including representatives of the Firmicutes (Bacillus, Sporosarcina, Viridibacillus, Paenibacillus, Staphylococcus and Brevibacillus) and Actinobacteria (Streptomyces). Non-spore forming organisms also survived, including Proteobacteria (Pseudomonas) and Actinobacteria (Arthrobacter) that are known to have environmentally resistant resting states. Clostridium spp. were isolated from the exposed soil under anaerobic culture. High NH3 was shown to cause a reduction in viability of spores over time, but spore morphology was not visibly altered. In addition to its implications for planetary protection, these data show that a large number of bacteria, potentially including spore-forming pathogens, but also environmentally resistant non-spore-formers, can survive high ammonia concentrations.

Keywords

ActinobacteriaammoniaClostridiumFirmicutesProteobacteriaspores
Type
Research Article
Information
International Journal of Astrobiology , Volume 11 , Issue 2 , April 2012 , pp. 125 - 131
Copyright
Copyright © Cambridge University Press 2012

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References

Angelidaki, I. & Ahring, B.K. (1993). Thermophilic anaerobic digestion of livestock waste the effect of ammonia. Appl. Microbiol. Biotechnol. 38, 560–564.Google Scholar
Braun, R., Huber, P. & Meyrath, J. (1981). Ammonia toxicity in liquid piggery manure digestion. Biotechnol. Lett. 3, 159–164.CrossRefGoogle Scholar
Brantley, S.L., Liermann, L., Bau, M. & Wu, S. (2001). Uptake of trace metals and rare earth elements from hornblende by a soil bacterium. Geomicrobiol. J. 18, 37–61.Google Scholar
Bruce, K.D., Hiorns, W.D., Hobman, J.L., Osborn, A.M., Strike, P. & Ritchie, D.A. (1992). Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl. Environ. Microbiol. 58, 3413–3416.Google Scholar
Cacciari, I. & Lippi, D. (1986). Arthrobacters, successful arid soil bacteria. A review. Arid Soil Res. Rehab. 1, 1–30.CrossRefGoogle Scholar
Cockell, C.S., Osinski, G.R., Banerjee, N.R., Howard, K.T., Gilmour, I. & Watson, J. (2010). The microbe–mineral environment and gypsum neogenesis in a weathered polar evaporite. Geobiology 8, 293–308.Google Scholar
Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Kulam-Syed-Mohideen, A.S., McGarrell, D.M., Marsh, T., Garrity, G.M. et al. (2009). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl. Acids Res. 37, D141–D145.CrossRefGoogle ScholarPubMed
Deal, P.H., Souza, K.A. & Mack, H.M. (1975). High pH, ammonia toxicity, and the search for life on the Jovian planets. Origins of Life 6, 561–573.Google Scholar
De Baere, L.A., Devocht, M., van Assche, P. & Verstrate, W. (1984). Influence of high NaCl and NH4Cl salt levels on methanogenic associations. Water Res. 18, 543–548.CrossRefGoogle Scholar
Fortes, A.D. (2000). Exobiological implications of a possible ammonia–water ocean inside Titan. Icarus 146, 444–452.CrossRefGoogle Scholar
Ghosh, S., Zhang, P., Li, Y.-Q. & Setlow, P. (2009). Superdormant spores of Bacillus species have elevated wet-heat resistance and temperature requirements for heat activation. J. Bacteriol. 191, 5584–5591.CrossRefGoogle ScholarPubMed
Gounot, A.M. (1967). Biologic role of Arthrobacter in subterranean soils. Ann Inst Pasteur Paris. 113, 923–945.Google Scholar
Hall, T.A. (1999). BioEdit; a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
Heyrman, J., Verbeeeren, J., Schumann, P., Swings, J. & De Vos, P. (2005). Six novel Arthrobacter species isolated from deteriorated mural paintings. Int. J. Syst. Evol. Microbiol. 55, 1457–1464.Google Scholar
Huertas, M.J., Duque, E., Marqués, S. & Ramos, J.L. (1998). Survival in soil of different toluene-degrading Pseudomonas strains after solvent shock. Appl. Environ. Microbiol. 64, 38–42.CrossRefGoogle ScholarPubMed
Jukes, T.H., Cantor, C.R. & Munro, H.N. (1969). Mammalian Protein Metabolism. Academic Press, New York, pp. 21–132.CrossRefGoogle Scholar
Koster, I.W. & Lettinga, G. (1984). The influence of ammonia–nitrogen on the specific activity of pellitized methanogenic sludge. Agric. Wastes 9, 205–216.CrossRefGoogle Scholar
La Duc, M.T., Osman, S., Vaishampayan, P., Piceno, Y., Andersen, G., Spry, J.A. & Venkateswaran, K. (2009). Comprehensive census of bacteria in clean rooms by using DNA microarray and cloning methods. Appl. Environ. Microbiol. 75, 6559–6567.Google Scholar
Mc Carty, P.L. & McKinney, R.E. (1961). Salt toxicity in anaerobic digestion. J. Water Pollut. Control Fed. 33, 399–415.Google Scholar
Mitri, G., Showman, A.P., Lunine, J.I. & Lopes, R.M.C. (2008). Resurfacing of Titan by ammonia–water cryomagma. Icarus 196, 216–224.CrossRefGoogle Scholar
Müller, T., Walter, B., Wirtz, A. & Burkovski, A. (2006). Ammonium toxicity in bacteria. Curr. Microbiol. 52, 400–406.CrossRefGoogle ScholarPubMed
Nelson, L.M. & Parkinson, D. (1978a). Growth characteristics of three bacterial isolates from an arctic soil. Can. J. Microbiol. 24, 909–914.CrossRefGoogle ScholarPubMed
Nelson, L.M. & Parkinson, D. (1978b). Effect of starvation on survival of three bacterial isolates from an arctic soil. Can. J. Microbiol. 24, 1460–1467.CrossRefGoogle ScholarPubMed
Preston, R.A. & Douthit, H.A. (1984). Stimulation of germination of unactivated Bacillus cereus spores by ammonia. J. Gen. Microbiol. 130, 1041–1050.Google Scholar
Reddy, G.S.N., Prakash, J.S.S., Matsumoto, G.I., Stackebrandt, E. & Shivaji, S. (2002). Arthrobacter roseus sp. nov., a psychrophilic bacterium isolated from an Antarctic cyanobacterial mat sample. Int. J. Syst. Evol. Microbiol. 52, 1017–1021.Google Scholar
Siegel, S.M. & Giumarro, C. (1965). Survival and growth of terrestrial microorganisms in ammonia-rich atmospheres. Icarus 40, 37–40.CrossRefGoogle Scholar
Siegel, S.M., Nathan, H.C. & Roberts, K. (1968). Experimental biology of ammonia-rich environments: optical and isotopic evidence for vital activity in Penicillium in liquid ammonia–glycerol at −40°C. Proc. Natl. Acad. Sci. USA 60, 505–508.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.CrossRefGoogle ScholarPubMed
Vishnivetskaya, T.A., Petrova, M.A., Urbance, J., Ponder, M., Moyer, C.L., Gilichinsky, D.A. & Tiedje, J.M. (2006). Bacterial community in ancient Siberian permafrost as characterised by culture and culture-independent methods. Astrobiology 6, 400–414.Google Scholar
Wolf, J. & Thorley, C.M. (1957). The effects of various germination agents on the spores of some strains of B. subtilis. J. Appl. Bacteriol. 20, 384–389.Google Scholar