Abstract
Organic and inorganic cyanides are widely distributed in nature, yet not much is known about the ability of microorganisms to use these compounds as a source of nitrogen and/or carbon at high temperatures (>80 °C). Here we studied the capacity of organic and inorganic cyanides to support growth of an hyperthermophilic Pyrococcus strain isolated from Deception Island, Antarctica. This microorganism was capable of growing with aromatic nitriles, aliphatic nitriles, heterocyclic nitriles, amino aromatic nitriles and inorganic cyanides as nitrogen and/or carbon source. This is the first report of an hyperthermophilic microorganism able to incorporate these compounds in its nitrogen and carbon metabolism. Based on enzymatic activity and genomic information, it is possibly that cells of this Pyrococcus strain growing with nitriles or cyanide, might use the carboxylic acid and/or the ammonia generated through the nitrilase enzymatic activity, as a carbon and/or nitrogen source respectively. This work expands the temperature range at which microorganisms can use organic and inorganic cyanides to growth, having important implications to understand microbial metabolisms that can support life on Earth and the possibility to support life elsewhere.
Similar content being viewed by others
Data availability
Unfortunately the genomic information of this strain is protected and this data is unavailble.
References
Amenabar MJ, Flores PA, Pugin B, Boehmwald FA, Blamey JM (2013) Archaeal diversity from hydrothermal systems of Deception Island. Antarct Polar Biol 36:373–380
Amenabar MJ, Martinez L, Yuan M, Contardo X, Cerpa LM, Rodrigo C, Blamey JM (2021) Role of chemosynthetic thermophilic communities on the biogeochemical cycles of minerals in the Orca Seamount area. Antarct Geomicrobiol J 38:859–868
Arrhenius GO (2003) Crystals and life. Helv Chim Acta 86:1569–1586
Bendia AG, Araujo GG, Pulschen AA, Contro B, Duarte RT, Rodrigues F, Galante D, Pellizari VH (2018) Surviving in hot and cold: psychrophiles and thermophiles from Deception Island volcano. Antarct Extrem 22:917–929
Bendia AG, Lemos LN, Mendes LW, Signori CN, Bohannan BJ, Pellizari VH (2021) Metabolic potential and survival strategies of microbial communities across extreme temperature gradients on Deception Island volcano. Antarct Environ Microbiol 23:4054–4073
Chen Z, Chen H, Ni Z, Tian R, Zhang T, Jia J, Yang S (2015) Expression and characterization of a novel nitrilase from hyperthermophilic bacterium Thermotoga maritima MSB8. J Microbiol Biotechnol 25:1660–1669
Correa-Llantén DN, Amenábar MJ, Muñoz PA, Monsalvez MT, Castro ME, Blamey JM (2014) Alicyclobacillus sp. strain CC2, a thermo-acidophilic bacterium isolated from Deception Island (Antarctica) containing a thermostable superoxide dismutase enzyme. Adv Polar Sci 25:92–96
Cramp R, Gilmour M, Cowan DA (1997) Novel thermophilic bacteria producing nitrile-degrading enzymes. Microbiology+ 143:2313–2320
Dennett GV, Blamey JM (2016) A new thermophilic nitrilase from an Antarctic hyperthermophilic microorganism. Front Bioeng Biotechnol 4:5
Fagerbakke KM, Heldal M, Norland S (1996) Content of carbon, nitrogen, oxygen, sulfur and phosphorus in native aquatic and cultured bacteria. Aquat Microb Ecol 10:15–27
Flores PA, Amenábar MJ, Blamey JM (2013) Hot environments from Antarctica: source of thermophiles and hyperthermophiles, with potential biotechnological applications. In: Thermophilic microbes in environmental and industrial biotechnology. Springer, Dordrecht, pp 99–118
Gavagan J, DiCosimo R, Eisenberg A, Fager S, Folsom P, Hann E, Schneider K, Fallon R (1999) A Gram-negative bacterium producing a heat-stable nitrilase highly active on aliphatic dinitriles. Appl Microbiol Biotechnol 52:654–659
Gong J-S, Lu Z-M, Li H, Shi J-S, Zhou Z-M, Xu Z-H (2012) Nitrilases in nitrile biocatalysis: recent progress and forthcoming research. Microb Cell Fact 11:1–18
Khawaja N, Postberg F, Hillier J, Klenner F, Kempf S, Nölle L, Reviol R, Zou Z, Srama R (2019) Low-mass nitrogen-, oxygen-bearing, and aromatic compounds in Enceladean ice grains. Mon Not R Astron Soc 489:5231–5243
Layh N, Hirrlinger B, Stolz A, Knackmuss H-J (1997) Enrichment strategies for nitrile-hydrolysing bacteria. Appl Microbiol Biotechnol 47:668–674
Legrain C, Demarez M, Glansdorff N, Piérard A (1995) Ammonia-dependent synthesis and metabolic channelling of carbamoyl phosphate in the hyperthermophilic archaeon Pyrococcus furiosus. Microbiology+ 141:1093–1099
Luthy RG, Bruce SG Jr (1979) Kinetics of reaction of cyanide and reduced sulfur species in aqueous solution. Environ Sci Technol 13:1481–1487
McKay C, Davila A, Glein C, Hand K, Stockton A (2018) Enceladus astrobiology, habitability, and the origin of life. In: Enceladus and the icy moons of Saturn. University of Arizona Press, Tucson, pp 437–452
Merino N, Aronson HS, Bojanova DP, Feyhl-Buska J, Wong ML, Zhang S, Giovannelli D (2019) Living at the extremes: extremophiles and the limits of life in a planetary context. Front Microbiol 10:780
Michoud G, Jebbar M (2016) High hydrostatic pressure adaptive strategies in an obligate piezophile Pyrococcus yayanosii. Sci Rep 6:27289
Mueller P, Egorova K, Vorgias CE, Boutou E, Trauthwein H, Verseck S, Antranikian G (2006) Cloning, overexpression, and characterization of a thermoactive nitrilase from the hyperthermophilic archaeon Pyrococcus abyssi. Protein Expr Purif 47:672–681
Neveu M, Anbar AD, Davila AF, Glavin DP, MacKenzie SM, Phillips-Lander CM, Sherwood B, Takano Y, Williams P, Yano H (2020) Returning samples from Enceladus for life detection. Front Astron Space Sci 7:26
Nissen LS, Basen M (2019) The emerging role of aldehyde: ferredoxin oxidoreductases in microbially-catalyzed alcohol production. J Biotechnol 306:105–117
Pereira RA, Graham D, Rainey FA, Cowan DA (1998) A novel thermostable nitrile hydratase. Extremophiles 2:347–357
Purcarea C, Simon V, Prieur D, Hervé G (1996) Purification and characterization of carbamoyl-phosphate synthetase from the deep-sea hyperthermophilic archaebacterium Pyrococcus abyssi. Eur J Biochem 236:189–199
Ray C, Glein CR, Waite JH, Teolis B, Hoehler T, Huber JA, Lunine J, Postberg F (2021) Oxidation processes diversify the metabolic menu on Enceladus. Icarus 364:114248
Searle PL (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review. Analyst 109:549–568
Somoza L, Martınez-Frıas J, Smellie J, Rey J, Maestro A (2004) Evidence for hydrothermal venting and sediment volcanism discharged after recent short-lived volcanic eruptions at Deception Island, Bransfield Strait, Antarctica. Mar Geol 203:119–140
Van den Ban EC, Willemen HM, Wassink H, Laane C, Haaker H (1999) Bioreduction of carboxylic acids by Pyrococcus furiosus in batch cultures. Enzyme Microb Technol 25:251–257
Verhoeven P, Hefter G, May P (1990) Dissociation constant of hydrogen cyanide in saline solutions. Min Met Explor 7:185–188
Wang Q, Sha C, Wang H, Ma K, Wiegle J, Abomohra AE-F, Shao W (2021) A novel bifunctional aldehyde/alcohol dehydrogenase catalyzing reduction of acetyl-CoA to ethanol at temperatures up to 95° C. Sci Rep 11:1050
Acknowledgements
We thank “Instituto Antártico Chileno” (INACH) for logistic support and permits during the Antarctic Chilean Expedition 46 (ECA46). We also thank the Spanish Antarctic Station “Gabriel de Castilla” for Antarctic field support. This research was funded by “Instituto Antártico Chileno” (INACH)”, “Fundación Científica y Cultural Biociencia” and by INNOVA-CORFO grant 07CN13PXT-264.
Funding
INNOVA-CORFO, 07CN13PXT-264, Fundación Científica y Cultural Biociencia, Instituto Antartico Chileno.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Communicated by Driessen.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Uribe-Redlich, P.A., Amenabar, M.J., Dennett, G.V. et al. Astrobiological implications of the organic and inorganic cyanide utilization by a novel Antarctic hyperthermophilic Pyrococcus strain. Extremophiles 28, 19 (2024). https://doi.org/10.1007/s00792-024-01335-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00792-024-01335-5