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Acid and aluminium-tolerant microbes isolated from China space station assembly cleanroom surfaces and identified by 16S rRNA/ITS sequencing and MALDI-TOF MS

Published online by Cambridge University Press:  03 March 2021

Nino Rcheulishvili Open the ORCID record for Nino Rcheulishvili [Opens in a new window] ,
Dimitri Papukashvili ,
Yasmeen Shakir ,
Yulin Deng  and
Ying Zhang
Nino Rcheulishvili
Affiliation:
School of Life Science, Beijing Institute of Technology, Beijing100081, China
Dimitri Papukashvili
Affiliation:
School of Life Science, Beijing Institute of Technology, Beijing100081, China
Yasmeen Shakir
Affiliation:
School of Life Science, Beijing Institute of Technology, Beijing100081, China
Yulin Deng*
Affiliation:
School of Life Science, Beijing Institute of Technology, Beijing100081, China Beijing Key Laboratory for Separation and Analysis in Biomedicine and Pharmaceuticals, Beijing100081, China
Ying Zhang*
Affiliation:
School of Life Science, Beijing Institute of Technology, Beijing100081, China Beijing Key Laboratory for Separation and Analysis in Biomedicine and Pharmaceuticals, Beijing100081, China
*
Author for correspondence: Yulin Deng, E-mail: [email protected]; Ying Zhang, E-mail: [email protected]
Author for correspondence: Yulin Deng, E-mail: [email protected]; Ying Zhang, E-mail: [email protected]
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Abstract

Corrosion of aluminium (Al) is a potential problem for spacecraft as this metal is used for various mechanical parts due to its strength, durability, etc. However, it can be corroded by certain factors including microbes. Studying microbes which can be implicated in microbiologically influenced corrosion (MIC) due to their extremophilic nature is of vital importance. In this current study, Al and acid-tolerant microbes were isolated from the samples of China space station assembly cleanroom surfaces; acidic environments can accelerate the corrosion process on metal surfaces. Nine bacterial and 10 fungal strains were identified with 16S ribosomal RNA gene/internal transcribed spacer region sequencing and matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. The dominant bacteria were of Bacillus, fungi of Penicillium and Aspergillus genera. Knowing the microbes which may be conveyed from the cleanrooms to the space stations with a potential capacity of Al degradation is important for long-term maintenance of station components. This study might aid in designing further researches of the aforementioned microorganisms and, therefore, contribute to the prevention of MIC.

Keywords

16S rRNA gene sequencingacid-tolerant microbesaluminium-corrosionMALDI-TOF MSmicrobiologically influenced corrosionspacecraft
Type
Research Article
Information
International Journal of Astrobiology , Volume 20 , Issue 2 , April 2021 , pp. 133 - 141
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abdolahi, A, Hamzah, E, Ibrahim, Z and Hashim, S (2014) Microbially influenced corrosion of steels by Pseudomonas aeruginosa. Corrosion Reviews 32, 129–141.CrossRefGoogle Scholar
Beech, IB and Sunner, J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Current Opinion in Biotechnology 15, 181–186.CrossRefGoogle ScholarPubMed
Broadbent, JR, Larsen, RL, Deibel, V and Steele, JL (2010) Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. Journal of Bacteriology 192, 2445–2458.CrossRefGoogle ScholarPubMed
Browne, N and Dowds, BCA (2002) Acid stress in the food pathogen Bacillus cereus. Journal of Applied Microbiology 92, 404–414.CrossRefGoogle ScholarPubMed
Calle, LM, Li, W, Buhrow, JW, Johansen, MR and Calle, CI (2018) Corrosion on Mars: an investigation of corrosion under relevant simulated Martian environments. 48th International Conference on Environmental Systems 8–12 July 2018, Albuquerque, New Mex ICES-2018–125.CrossRefGoogle Scholar
Castaneda, H and Benetton, XD (2008) SRB-biofilm influence in active corrosion sites formed at the steel-electrolyte interface when exposed to artificial seawater conditions. Corrosion Science 50, 1169–1183.CrossRefGoogle Scholar
Checinska, A, Probst, AJ, Vaishampayan, P, White, JR, Kumar, D, Stepanov, VG, Fox, GE, Nilsson, HR, Pierson, DL, Perry, J and Venkateswaran, K (2015) Microbiomes of the dust particles collected from the International Space Station and Spacecraft Assembly Facilities. Microbiome 3, 50.CrossRefGoogle ScholarPubMed
Checinska Sielaff, A, Urbaniak, C, Mohan, GBM, Stepanov, VG, Tran, Q, Wood, JM, Minich, J, McDonald, D, Mayer, T, Knight, R, Karouia, F, Fox, GE and Venkateswaran, K (2019) Characterization of the total and viable bacterial and fungal communities associated with the International Space Station surfaces. Microbiome 7, 50.CrossRefGoogle ScholarPubMed
Cortesão, M, Fuchs, FM, Commichau, FM, Eichenberger, P, Schuerger, AC, Nicholson, WL, Setlow, P and Moeller, R (2019) Bacillus subtilis spore resistance to simulated Mars surface conditions. Frontiers in Microbiology 10, 333.CrossRefGoogle ScholarPubMed
Dai, X, Wang, H, Ju, LK, Cheng, G, Cong, H and Newby, BMZ (2017) Corrosion of aluminum alloy 2024 caused by Aspergillus niger. International Biodeterioration and Biodegradation 115, 1–10.CrossRefGoogle Scholar
Dingle, TC and Butler-Wu, SM (2013) MALDI-TOF mass spectrometry for microorganism identification. Clinics in Laboratory Medicine 33, 589–609.CrossRefGoogle ScholarPubMed
ECSS ESA for the members of (2008) Microbial examination of flight hardware and cleanrooms. ESA Requir Stand Div ESTEC, P.O:ECSS-Q-ST-70-55C.Google Scholar
Fajardo-Cavazos, P, Narvel, R and Nicholson, WL (2014) Differing responses in growth and spontaneous mutation to antibiotic resistance in Bacillus subtilis and Staphylococcus epidermidis cells exposed to simulated microgravity. Gravitational and Space Research 2, 2.CrossRefGoogle Scholar
Farrell, MJ and Finkel, SE (2003) The growth advantage in stationary-phase phenotype conferred by rpoS mutations is dependent on the pH and nutrient environment. Journal of Bacteriology 185, 7044–7052.CrossRefGoogle Scholar
Gabani, P, Copeland, E, Chandel, AK and Singh, OV (2012) Ultraviolet-radiation-resistant isolates revealed cellulose-degrading species of Cellulosimicrobium cellulans (UVP 1) and Bacillus pumilus (UVP 4). Biotechnology and Applied Biochemistry 59, 395–404.CrossRefGoogle Scholar
Ghosh, S, Osman, S, Vaishampayan, P and Venkateswaran, K (2010) From the clean room where Phoenix spacecraft components were assembled. Astrobiology 10, 325–335.CrossRefGoogle ScholarPubMed
Glukhova, LB, Frank, YA, Danilova, EV, Avakyan, MR, Banks, D, Tuovinen, OH and Karnachuk, OV (2018) Isolation, characterization, and metal response of novel, acid-tolerant Penicillium spp. from extremely metal-rich waters at a mining site in Transbaikal (Siberia, Russia). Microbial Ecology 76, 911–924.CrossRefGoogle Scholar
Goswami, G, Panda, D, Samanta, R, Boro, RC, Modi, MK, Bujarbaruah, KM and Barooah, M (2018) Bacillus megaterium adapts to acid stress condition through a network of genes: insight from a genome-wide transcriptome analysis. Scientific Reports 8, 16105.CrossRefGoogle ScholarPubMed
Gu, T and Galicia, B (2012) Can acid producing bacteria be responsible for very fast MIC pitting? Corros. 2012 NACE Corrosion/2012, No. C2012-0001214, S March 11.Google Scholar
Gu, T, Xu, D, Zhang, P, Li, Y and Lindenberger, AL (2015) Microbiologically influenced corrosion and its impact on metals and other materials. Microbiology for Minerals, Metals, Materials and the Environment 25, 383–408.Google Scholar
Henning, C, Vijayakumar, P, Adhikari, R, Jagannathan, B, Gautam, D and Muriana, PM (2015) Isolation and taxonomic identity of bacteriocin-producing lactic acid bacteria from retail foods and animal sources. Microorganisms 3, 80–93.CrossRefGoogle ScholarPubMed
Ichijo, T, Yamaguchi, N, Tanigaki, F, Shirakawa, M and Nasu, M (2016) Four-year bacterial monitoring in the International Space Station – Japanese experiment module ‘Kibo’ with culture-independent approach. NPJ Microgravity 2, 16007.CrossRefGoogle ScholarPubMed
Jang, KS and Kim, YH (2018) Rapid and robust MALDI-TOF MS techniques for microbial identification: a brief overview of their diverse applications. Journal of Microbiol 56, 209–216.CrossRefGoogle ScholarPubMed
Jirón-Lazos, U, Corvo, F, De la Rosa, SC, García-Ochoa, EM, Bastidas, DM and Bastidas, JM (2018) Localized corrosion of aluminum alloy 6061 in the presence of Aspergillus niger. International Biodeterioration & Biodegradation 133, 17–25.CrossRefGoogle Scholar
Kacena, MA, Merrell, GA, Manfredi, B, Smith, EE, Klaus, DM and Todd, P (1999) Bacterial growth in space flight: logistic growth curve parameters for Escherichia coli and Bacillus subtilis. Applied Microbiology and Biotechnology 51, 229–234.CrossRefGoogle ScholarPubMed
Karn, SK, Fang, G and Duan, J (2017) Bacillus sp. acting as dual role for corrosion induction and corrosion inhibition with carbon steel (CS). Frontiers in Microbiology 8, 2038.CrossRefGoogle Scholar
Kawai, F, Zhang, D and Sugimoto, M (2000) Isolation and characterization of acid- and Al-tolerant microorganisms. FEMS Microbiology Letters 189, 143–147.CrossRefGoogle ScholarPubMed
Kim, W, Tengra, FK, Young, Z, Shong, J, Marchand, N, Chan, HK, Pangule, RC, Parra, M, Dordick, JS, Plawsky, JL and Collins, CH (2013) Spaceflight promotes biofilm formation by Pseudomonas aeruginosa. PLoS ONE 8, e62437.CrossRefGoogle ScholarPubMed
Klintworth, R, Reher, HJ, Viktorov, AN and Bohle, D (1999) Biological induced corrosion of materials II: new test methods and experiences from MIR station. Acta Astronautica 44, 569–578.CrossRefGoogle ScholarPubMed
Knox, BP, Blachowicz, A, Palmer, JN, Romsdahl, J, Huttenlocher, A, Wang, CCC, Keller, NP and Venkateswaran, K (2016) Characterization of Aspergillus fumigatus isolates from air and surfaces of the international space station. mSphere 1, e00227–16.CrossRefGoogle ScholarPubMed
Koskinen, K, Rettberg, P, Pukall, R, Auerbach, A, Wink, L, Barczyk, S, Perras, A, Mahnert, A, Margheritis, D, Kminek, G and Moissl-Eichinger, C (2017) Microbial biodiversity assessment of the European Space Agency's ExoMars 2016 mission. Microbiome 5, 143.CrossRefGoogle ScholarPubMed
Kryachko, Y and Hemmingsen, SM (2017) The role of localized acidity generation in microbially influenced corrosion. Current Microbiology 74, 870–876.CrossRefGoogle ScholarPubMed
Kumar, M and Shukla, PK (2005) Use of PCR targeting of internal transcribed spacer regions and single-stranded conformation polymorphism analysis of sequence variation in different regions of rRNA genes in fungi for rapid diagnosis of mycotic keratitis. Journal of Clinical Microbiology 43, 662–668.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kunito, T, Isomura, I, Sumi, H, Park, HD, Toda, H, Otsuka, S, Nagaoka, K, Saeki, K and Senoo, K (2016) Aluminum and acidity suppress microbial activity and biomass in acidic forest soils. Soil Biology and Biochemistry 97, 23–30.CrossRefGoogle Scholar
Kwan, K, Cooper, M, La Duc, MT, Vaishampayan, P, Stam, C, Benardini, JN, Scalzi, G, Moissl-Eichinger, C and Venkateswaran, K (2011) Evaluation of procedures for the collection, processing, and analysis of biomolecules from low-biomass surfaces. Applied and Environmental Microbiology 77, 2943–2953.CrossRefGoogle ScholarPubMed
La Duc, MT, Dekas, A, Osman, S, Moissl, C, Newcombe, D and Venkateswaran, K (2007) Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Applied and Environmental Microbiology 73, 2600–2611.CrossRefGoogle ScholarPubMed
Lang, JM, Coil, DA, Neches, RY, Brown, WE, Cavalier, D, Severance, M, Hampton-Marcell, JT, Gilbert, JA and Eisen, JA (2017) A microbial survey of the International Space Station (ISS). PeerJ 5, e4029.CrossRefGoogle Scholar
Liu, T, Wang, Y, Pan, S, Zhao, Q, Zhan, C, Gao, S, Guo, Z, Guo, N, Sand, W, Chang, X, Dong, L and Yin, Y (2019) The addition of copper accelerates the corrosion of steel via impeding biomineralized film formation of Bacillus subtilis in seawater. Corrosion Science 149, 153–163.CrossRefGoogle Scholar
Macdonald, TL and Martin, RB (1988) Aluminum ion in biological systems. Trends in Biochemical Sciences 13, 15–19.CrossRefGoogle ScholarPubMed
Martin, RB (1986) The chemistry of aluminum as related to biology and medicine. Clinical Chemistry 32, 1797–1806.CrossRefGoogle ScholarPubMed
Maurer, LM, Yohannes, E, Bondurant, SS, Radmacher, M and Slonczewski, JL (2005) Ph regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. Journal of Bacteriology 187, 304–319.CrossRefGoogle ScholarPubMed
Mori, M, Gomi, M, Matsumune, N, Niizeki, K and Sakagami, Y (2013) Biofilm-forming activity of bacteria isolated from toilet bowl biofilms and the bactericidal activity of disinfectants against the isolates. Biocontrol Science 18, 129–135.CrossRefGoogle ScholarPubMed
Moura, MC, Pontual, EV, Paiva, PMG and Coelho, LCBB (2013) An outline to corrosive Bacteria. In Méndez-Vilas, A (ed). Microbial Pathogens and Strategies for Combating Them: Science, Technology and Education. Badajoz, Spain: Formatex Research Centre, pp. 11–22.Google Scholar
Nadir, AJ (2017) A hitchhiker's guide to an ISS experiment in under 9 months. NPJ Microgravity 3, 1–10.Google Scholar
Neuberger, K, Lux-Endrich, A, Panitz, C and Horneck, G (2015) Survival of spores of Trichoderma longibrachiatum in space: data from the space experiment SPORES on EXPOSE-R. International Journal of Astrobiology 14, 129–113.CrossRefGoogle Scholar
Novikova, N (2004) Review of the knowledge of microbial contamination of the Russian manned spacecraft. Microbial Ecology 47, 127–132.CrossRefGoogle ScholarPubMed
Novikova, N, De Boever, P, Poddubko, S, Deshevaya, E, Polikarpov, N, Rakova, N, Coninx, I and Mergeay, M (2006) Survey of environmental biocontamination on board the International Space Station. Research in Microbiology 157, 5–12.CrossRefGoogle ScholarPubMed
Parfitt, T (2005) Georgia: an unlikely stronghold for bacteriophage therapy. Lancet (London, England) 365, 2166–2167.CrossRefGoogle ScholarPubMed
Pedramfar, A, Maal, KB and Mirdamadian, SH (2017) Phage therapy of corrosion-producing bacterium Stenotrophomonas maltophilia using isolated lytic bacteriophages. Anti-Corrosion Methods and Materials 64, 607–612.CrossRefGoogle Scholar
Pina, RG and Cervantes, C (1996) Microbial interactions with aluminium. Biometals 9, 311–316.CrossRefGoogle ScholarPubMed
Popović, T, Ivanović, Ž, Živković, S, Trkulja, N and Ignjatov, M (2013) First report of Brenneria nigrifluens as the causal agent of shallow-bark canker on walnut trees (Juglans regia) in Serbia. Plant Disease 97, 1504.CrossRefGoogle Scholar
Rahi, P, Prakash, O and Shouche, YS (2016) Matrix-assisted laser desorption/ionization time-of-flight mass-spectrometry (MALDI-TOF MS) based microbial identifications: challenges and scopes for microbial ecologists. Frontiers in Microbiology 7, 1359.CrossRefGoogle ScholarPubMed
Rajasekar, A and Ting, YP (2010) Microbial corrosion of aluminum 2024 aeronautical alloy by hydrocarbon degrading bacteria Bacillus cereus ACE4 and Serratia marcescens ACE2. Industrial & Engineering Chemistry Research 49, 6054–6061.CrossRefGoogle Scholar
Reidt, U, Helwig, A, Müller, G, Plobner, L, Lugmayr, V, Kharin, S, Smirnov, Y, Novikova, N, Lenic, J, Fetter, V and Hummel, T (2017) Detection of microorganisms onboard the international space station using an electronic nose. Gravitational and Space Research 5, 89–111.CrossRefGoogle Scholar
Rychert, J (2019) Benefits and limitations of MALDI-TOF mass spectrometry for the identification of microorganisms. Journal of Infection 2, 1–5.Google Scholar
Satoh, K, Yamazaki, T, Nakayama, T, Umeda, Y, Alshahni, MM, Makimura, M and Makimura, K (2016) Characterization of fungi isolated from the equipment used in the International Space Station or Space Shuttle. Microbiology and Immunology 60, 295–302.CrossRefGoogle ScholarPubMed
Sauer, S, Freiwald, A, Maier, T, Kube, M, Reinhardt, R, Kostrzewa, M and Geider, K (2008) Classification and identification of bacteria by mass spectrometry and computational analysis. PLoS ONE 3, e2843.CrossRefGoogle ScholarPubMed
Schwendner, P, Moissl-Eichinger, C, Barczyk, S, Bohmeier, M, Pukall, R and Rettberg, P (2013) Insights into the microbial diversity and bioburden in a South American spacecraft assembly clean room. Astrobiology 13, 1140–1154.CrossRefGoogle Scholar
Seuylemezian, A, Aronson, HS, Tan, J, Lin, M, Schubert, W and Vaishampayan, P (2018) Development of a custom MALDI-TOF MS database for species-level identification of bacterial isolates collected from spacecraft and associated surfaces. Frontiers in Microbiology 9, 780.CrossRefGoogle ScholarPubMed
Singhal, N, Kumar, M, Kanaujia, PK and Virdi, JS (2015) MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Frontiers in Microbiology 6, 791.CrossRefGoogle ScholarPubMed
Smirnov, VF, Belov, DV, Sokolova, TN, Kuzina, OV and Kartashov, VR (2008) Microbiological corrosion of aluminum alloys. Applied Biochemistry and Microbiology 44, 192–196.CrossRefGoogle ScholarPubMed
Sören Schubert, K and Kostrzewa, M (2017) MALDI-TOF MS in microbiology laboratory: current trends. Current Issues in Molecular Biology 23, 17–20.CrossRefGoogle Scholar
Stieglmeier, M, Rettberg, P, Barczyk, S, Bohmeier, M, Pukall, R, Wirth, R and Moissl-Eichinger, C (2012) Abundance and diversity of microbial inhabitants in European spacecraft-associated clean rooms. Astrobiology 12, 572–585.CrossRefGoogle ScholarPubMed
Telegdi, J, Shaban, A and Trif, L (2017) Microbiologically influenced corrosion (MIC). In El-Sherik, AM (ed). Trends Oil and Gas Corrosion Research and Technologies. Cambridge, England: Elsevier Ltd, pp. 191–214.CrossRefGoogle Scholar
Thomassin, S, Jobin, MP and Schmitt, P (2006) The acid tolerance response of Bacillus cereus ATCC14579 is dependent on culture pH, growth rate and intracellular pH. Archives of Microbiology 186, 229–239.CrossRefGoogle ScholarPubMed
Torres-Barceló, C (2018) The disparate effects of bacteriophages on antibiotic-resistant bacteria. Emerging Microbes & Infections 7, 168.CrossRefGoogle ScholarPubMed
Tucker, DL, Tucker, N and Conway, T (2002) Gene expression profiling of the pH response in Escherichia coli. Journal of Bacteriology 184, 6551–6558.CrossRefGoogle Scholar
Venkateswaran, K, Vaishampayan, P, Cisneros, J, Pierson, DL, Rogers, SO and Perry, J (2014) International Space Station environmental microbiome – microbial inventories of ISS filter debris. Applied Microbiology and Biotechnology 98, 6453–6466.CrossRefGoogle ScholarPubMed
Videla, HA and Herrera, LK (2005) Microbiologically influenced corrosion: looking to the future. International Microbiology 8, 169–180.Google Scholar
Voorhies, AA, Mark Ott, C, Mehta, S, Pierson, DL, Crucian, BE, Feiveson, A, Oubre, CM, Torralba, M, Moncera, K, Zhang, Y, Zurek, E and Lorenzi, HA (2019) Study of the impact of long-duration space missions at the International Space Station on the astronaut microbiome. Scientific Reports 9, 9911.CrossRefGoogle ScholarPubMed
Walch, G, Knapp, M, Rainer, G and Peintner, U (2016) Colony-PCR is a rapid method for DNA amplification of hyphomycetes. Journal of Fungi 2, 12.CrossRefGoogle ScholarPubMed
Welker, M, Van Belkum, A, Girard, V, Charrier, JP and Pincus, D (2019) An update on the routine application of MALDI-TOF MS in clinical microbiology. Expert Review of Proteomics 16, 695–710.CrossRefGoogle ScholarPubMed
Xu, D, Li, Y, Song, F and Gu, T (2013) Laboratory investigation of microbiologically influenced corrosion of C1018 carbon steel by nitrate reducing bacterium Bacillus licheniformis. Corrosion Science 77, 385–390.CrossRefGoogle Scholar
Yang, SS, Chen, CY, Wei, CB and Lin, YT (1996) Microbial corrosion of aluminum alloy. Chinese Journal of Microbiology and Immunology 29, 185–196.Google ScholarPubMed
Yang, SS, Lin, JY and Lin, YT (1998) Microbiologically induced corrosion of aluminum alloys in fuel-oil/aqueous system. Journal of Microbiology, Immunology and Infection 31, 151–164.Google ScholarPubMed
Zarrin, M, Ganj, F and Faramarzi, S (2016) Analysis of the rDNA internal transcribed spacer region of the Fusarium species by polymerase chain reaction – restriction fragment length polymorphism. Biomedical Reports 4, 471–474.CrossRefGoogle ScholarPubMed
Zea, L, Nisar, Z, Rubin, P, Cortesão, M, Luo, J, McBride, SA, Moeller, R, Klaus, D, Müller, D, Varanasi, KK, Muecklich, F and Stodieck, L (2018) Design of a spaceflight biofilm experiment. Acta Astronautica 148, 294–300.CrossRefGoogle ScholarPubMed
Zhang, YJ, Zhang, S, Liu, XZ, Wen, HA and Wang, M (2010) A simple method of genomic DNA extraction suitable for analysis of bulk fungal strains. Letters in Applied Microbiology 51, 114–118.Google ScholarPubMed
Zhang, Y, Zhang, LT, Li, ZD, Xin, CS, Li, XQ, Wang, X and Deng, YL (2019) Microbiomes of China's Space Station during assembly, integration, and test operations. Microbial Ecology 78, 631–650.CrossRefGoogle ScholarPubMed