Growth and biofilm formation of Cupriavidus metallidurans CH34 on different metallic and polymeric materials used in spaceflight applications

References

• Acres JM, Youngapelian MJ, Nadeau J. 2021. The influence of spaceflight and simulated microgravity on bacterial motility and chemotaxis. NPJ Microgravity. 7:7. doi:10.1038/s41526-021-00135-x
   PubMed Web of Science ®Google Scholar
• Alfa MJ, Ribeiro MM, da Costa Luciano C, Franca R, Olson N, DeGagne P, Singh H. 2017. A novel polytetrafluoroethylene-channel model, which simulates low levels of culturable bacteria in buildup biofilm after repeated endoscope reprocessing. Gastrointest Endosc. 86:442–451 e441. doi:10.1016/j.gie.2017.05.014
   PubMed Web of Science ®Google Scholar
• Bakker DP, Busscher HJ, van der Mei HC. 2002. Bacterial deposition in a parallel plate and a stagnation point flow chamber: microbial adhesion mechanisms depend on the mass transport conditions. Microbiology (Reading). 148:597–603. doi:10.1099/00221287-148-2-597
   PubMed Web of Science ®Google Scholar
• Barnes AM, Ballering KS, Leibman RS, Wells CL, Dunny GM. 2012. Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. mBio. 3:e00193-00112. doi:10.1128/mBio.00193-12
   Web of Science ®Google Scholar
• Berggren D, Bertling S, Heijerick D, Herting G, Koundakjian P, Leygraf C, Odnevall Wallinder I. 2004. Release of chromium, nickel and iron from stainless steel exposed under atmospheric conditions and the environmental interaction of these metals: a combined field and laboratory investigation, Eurofer and Swedish Steel Association.
   Google Scholar
• Bijlani S, Stephens E, Singh NK, Venkateswaran K, Wang CCC. 2021. Advances in space microbiology. iScience. 24:102395. doi:10.1016/j.isci.2021.102395
   PubMed Web of Science ®Google Scholar
• Buzzo JR, Devaraj A, Gloag ES, Jurcisek JA, Robledo-Avila F, Kesler T, Wilbanks K, Mashburn-Warren L, Balu S, Wickham J, et al. 2021. Z-form extracellular DNA is a structural component of the bacterial biofilm matrix. Cell. 184:5740–5758. e5717doi:10.1016/j.cell.2021.10.010.
   PubMed Web of Science ®Google Scholar
• Byloos B, Coninx I, Van Hoey O, Cockell C, Nicholson N, Ilyin V, Van Houdt R, Boon N, Leys N. 2017. The impact of space flight on survival and interaction of Cupriavidus metallidurans CH34 with Basalt, a Volcanic Moon Analog Rock. Front Microbiol. 8:671. doi:10.3389/fmicb.2017.00671
   PubMed Web of Science ®Google Scholar
• Campoccia D, Montanaro L, Arciola CR. 2021. Extracellular DNA (eDNA). A major ubiquitous element of the bacterial biofilm architecture. IJMS. 22:9100. doi:10.3390/ijms22169100
   Google Scholar
• Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J. 2005. Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Res Microbiol. 156:506–514. doi:10.1016/j.resmic.2005.01.007
   PubMed Web of Science ®Google Scholar
• Chen G, Walker SL. 2007. Role of solution chemistry and ion valence on the adhesion kinetics of groundwater and marine bacteria. Langmuir. 23:7162–7169. doi:10.1021/la0632833
   PubMed Web of Science ®Google Scholar
• Cockell CS, Santomartino R, Finster K, Waajen AC, Eades LJ, Moeller R, Rettberg P, Fuchs FM, Van Houdt R, Leys N, et al. 2020. Space station biomining experiment demonstrates rare earth element extraction in microgravity and Mars gravity. Nat Commun. 11:5523. doi:10.1038/s41467-020-19276-w
   PubMed Web of Science ®Google Scholar
• Cwalina B, Dec W, Michalska JK, Jaworska-Kik M, Student S. 2017. Initial stage of the biofilm formation on the NiTi and Ti6Al4V surface by the sulphur-oxidizing bacteria and sulphate-reducing bacteria. J Mater Sci Mater Med. 28:173. doi:10.1007/s10856-017-5988-2
   PubMed Web of Science ®Google Scholar
• Das T, Sharma PK, Busscher HJ, van der Mei HC, Krom BP. 2010. Role of extracellular DNA in initial bacterial adhesion and surface aggregation. Appl Environ Microbiol. 76:3405–3408. doi:10.1128/AEM.03119-09
   PubMed Web of Science ®Google Scholar
• De Gelder J, Vandenabeele P, De Boever P, Mergeay M, Moens L, De Vos P. 2009. Raman spectroscopic analysis of Cupriavidus metallidurans LMG 1195 (CH34) cultured in low-shear microgravity conditions. Microgravity Sci Technol. 21:217–223. doi:10.1007/s12217-008-9037-0
   Web of Science ®Google Scholar
• Diaz A, Li W, Irwin TD, Calle LM, Callahan MR. 2019. Investigation of biofilm formation and control for spacecraft – an early literature review. 49th International Conference on Environmental Systems. Boston, Massachusetts.
   Google Scholar
• Flemming HC. 1998. Relevance of biofilms for the biodeterioration of surfaces of polymeric materials. Polym Degrad Stab. 59:309–315.
   Web of Science ®Google Scholar
• Guan N, Liu L. 2020. Microbial response to acid stress: mechanisms and applications. Appl Microbiol Biotechnol. 104:51–65. doi:10.1007/s00253-019-10226-1
   PubMed Web of Science ®Google Scholar
• Gyo M, Nikaido T, Okada K, Yamauchi J, Tagami J, Matin K. 2008. Surface response of fluorine polymer-incorporated resin composites to cariogenic biofilm adherence. Appl Environ Microbiol. 74:1428–1435. doi:10.1128/AEM.02039-07
   PubMed Web of Science ®Google Scholar
• Gyurcsik B, Nagy L. 2000. Carbohydrates as ligands: coordination equilibria and structure of the metal complexes. Coord Chem Rev. 203:81–149. doi:10.1016/S0010-8545(99)00183-6
   Web of Science ®Google Scholar
• Hamadi F, Latrache H, Zekraoui M, Ellouali M, Bengourram J. 2009. Effect of pH on surface energy of glass and Teflon and theoretical prediction of Staphylococcus aureus adhesion. Mater Sci Eng C. 29:1302–1305. doi:10.1016/j.msec.2008.10.023
   Web of Science ®Google Scholar
• Harrison JJ, Ceri H, Turner RJ. 2007. Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol. 5:928–938. doi:10.1038/nrmicro1774
   PubMed Web of Science ®Google Scholar
• Hedberg YS, Odnevall Wallinder I. 2015. Metal release from stainless steel in biological environments: a review. Biointerphases. 11:018901. doi:10.1116/1.4934628
   PubMed Web of Science ®Google Scholar
• Herting G, Wallinder IO, Leygraf C. 2006. Factors that influence the release of metals from stainless steels exposed to physiological media. Corros. Sci. 48:2120–2132. doi:10.1016/j.corsci.2005.08.006
   Web of Science ®Google Scholar
• Horneck G, Klaus DM, Mancinelli RL. 2010. Space microbiology. Microbiol Mol Biol Rev. 74:121–156. doi:10.1128/MMBR.00016-09
   PubMed Web of Science ®Google Scholar
• Huang B, Li DG, Huang Y, Liu CT. 2018. Effects of spaceflight and simulated microgravity on microbial growth and secondary metabolism. Mil Med Res. 5:18. doi:10.1186/s40779-018-0162-9
   PubMed Web of Science ®Google Scholar
• Ibanez de Aldecoa AL, Zafra O, Gonzalez-Pastor JE. 2017. Mechanisms and regulation of extracellular DNA release and its biological roles in microbial communities. Front Microbiol. 8:1390. doi:10.3389/fmicb.2017.01390
   PubMed Web of Science ®Google Scholar
• Ishida Y, Kadota H. 1981. Growth patterns and substrate requirements of naturally occurring obligate oligotrophs. Microb Ecol. 7:123–130. doi:10.1007/BF02032494
   PubMed Web of Science ®Google Scholar
• Jacobsen M, Clausen PP, Smidth S. 1980. The effect of fixation and trypsinization on the immunohistochemical demonstration of intracellular immunoglobulin in paraffin embedded material. Acta Pathol Microbiol Scand A. 88:369–376. doi:10.1111/j.1699-0463.1980.tb02508.x
   PubMedGoogle Scholar
• Kim M, Jeon J, Kim J. 2018. Streptococcus mutans extracellular DNA levels depend on the number of bacteria in a biofilm. Sci. Rep. 8:13313. doi:10.1038/s41598-018-31275-y
   PubMed Web of Science ®Google Scholar
• Klintworth R, Reher HJ, Viktorov AN, Bohle D. 1999. Biological induced corrosion of materials II: new test methods and experiences from MIR station. Acta Astronaut. 44:569–578. doi:10.1016/S0094-5765(99)00069-7
   PubMed Web of Science ®Google Scholar
• Leroy B, Rosier C, Erculisse V, Leys N, Mergeay M, Wattiez R. 2010. Differential proteomic analysis using isotope-coded protein-labeling strategies: comparison, improvements and application to simulated microgravity effect on Cupriavidus metallidurans CH34. Proteomics. 10:2281–2291. doi:10.1002/pmic.200900286
   PubMed Web of Science ®Google Scholar
• Leys N, Baatout S, Rosier C, Dams A, s'Heeren C, Wattiez R, Mergeay M. 2009. The response of Cupriavidus metallidurans CH34 to spaceflight in the international space station. Antonie Van Leeuwenhoek. 96:227–245. doi:10.1007/s10482-009-9360-5
   PubMed Web of Science ®Google Scholar
• Liu J, Madec JY, Bousquet-Melou A, Haenni M, Ferran AA. 2021. Destruction of Staphylococcus aureus biofilms by combining an antibiotic with subtilisin A or calcium gluconate. Sci Rep. 11:6225. doi:10.1038/s41598-021-85722-4
   PubMed Web of Science ®Google Scholar
• Luo TL, Hayashi M, Zsiska M, Circello B, Eisenberg M, Gonzalez-Cabezas C, Foxman B, Marrs CF, Rickard AH. 2019. Introducing BAIT (Biofilm Architecture Inference Tool): a software program to evaluate the architecture of oral multi-species biofilms. Microbiology (Reading). 165:527–537. doi:10.1099/mic.0.000761
   PubMed Web of Science ®Google Scholar
• Maertens L, Coninx I, Claesen J, Leys N, Matroule JY, Van Houdt R. 2020. Copper resistance mediates long-term survival of Cupriavidus metallidurans in wet contact with metallic copper. Front Microbiol. 11:1208. doi:10.3389/fmicb.2020.01208
   PubMed Web of Science ®Google Scholar
• Mah TF, O'Toole GA. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34–39. doi:10.1016/S0966-842X(00)01913-2
   PubMed Web of Science ®Google Scholar
• Maryatt BW. 2018. Lessons learned for the international space station potable water dispenser. 48th International Conference on Environmental Systems. Albuquerque, New Mexico.
   Google Scholar
• Mergeay M. 1995. Heavy metal resistances in microbial ecosystems. In Akkermans, ADL, Van Elsas, JD, De Bruijn, FJ, editors. Molecular microbial ecology manual. Dordrecht: Springer; p. 439–455. doi:10.1007/978-94-011-0351-0_30
   Google Scholar
• Mergeay M, Nies D, Schlegel HG, Gerits J, Charles P, Van Gijsegem F. 1985. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol. 162:328–334. doi:10.1128/jb.162.1.328-334.1985
   PubMed Web of Science ®Google Scholar
• Mijnendonckx K, Ali MM, Provoost A, Janssen P, Mergeay M, Leys N, Charlier D, Monsieurs P, Van Houdt R. 2019. Spontaneous mutation in the AgrRS two-component regulatory system of Cupriavidus metallidurans results in enhanced silver resistance. Metallomics. 11:1912–1924. doi:10.1039/c9mt00123a
   PubMed Web of Science ®Google Scholar
• Mijnendonckx K, Provoost A, Ott CM, Venkateswaran K, Mahillon J, Leys N, Van Houdt R. 2013. Characterization of the survival ability of Cupriavidus metallidurans and Ralstonia pickettii from space-related environments. Microb Ecol. 65:347–360. doi:10.1007/s00248-012-0139-2
   PubMed Web of Science ®Google Scholar
• Minh Tran T, MacIntyre A, Khokhani D, Hawes M, Allen C. 2016. Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence. Environ Microbiol. 18:4103–4117. doi:10.1111/1462-2920.13446
   PubMed Web of Science ®Google Scholar
• Mumme T, Müller-Rath R, Jakobi N, Weißkopf M, Dott W, Marx R, Wirtz D-C. 2005. In vitro serum levels of metal ions released from orthopaedic implants. Eur J Orthop Surg Traumatol. 15:83–89. doi:10.1007/s00590-004-0206-6
   Google Scholar
• National Research Council. 2000. Methods for developing spacecraft water exposure guidelines. Washington, DC: The National Academies Press. doi:10.17226/9892
   Google Scholar
• Okshevsky M, Meyer RL. 2015. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol. 41:341–352. doi:10.3109/1040841X.2013.841639
   PubMed Web of Science ®Google Scholar
• Okshevsky M, Regina VR, Meyer RL. 2015. Extracellular DNA as a target for biofilm control. Curr Opin Biotechnol. 33:73–80. doi:10.1016/j.copbio.2014.12.002
   PubMed Web of Science ®Google Scholar
• Padan E, Bibi E, Ito M, Krulwich TA. 2005. Alkaline pH homeostasis in bacteria: new insights. Biochim Biophys Acta. 1717:67–88. doi:10.1016/j.bbamem.2005.09.010
   PubMed Web of Science ®Google Scholar
• Pal A, Paul AK. 2013. Optimization of cultural conditions for production of extracellular polymeric substances (EPS) by Serpentine Rhizobacterium Cupriavidus pauculus KPS 201. J Polym. 2013:1–7. doi:10.1155/2013/692374
   Google Scholar
• Panlilio H, Rice CV. 2021. The role of extracellular DNA in the formation, architecture, stability, and treatment of bacterial biofilms. Biotechnol Bioeng. 118:2129–2141. doi:10.1002/bit.27760
   PubMed Web of Science ®Google Scholar
• Percival S. 1999. The effect of molybdenum on biofilm development. J Ind Microbiol Biotechnol. 23:112–117. doi:10.1038/sj.jim.2900712
   PubMed Web of Science ®Google Scholar
• Percival SL, Beech IB, Edyvean RGJ, Knapp JS, Wales DS. 1997. Biofilm development on 304 and 316 stainless steels in a potable water system. Water & Environment J. 11:289–294. doi:10.1111/j.1747-6593.1997.tb00131.x
   Web of Science ®Google Scholar
• Petala M, Tsiridis V, Darakas E, Kostoglou M. 2020. Longevity aspects of potable water disinfected by ionic silver: kinetic experiments and modeling. Water. 12:258. doi:10.3390/w12010258.
   Web of Science ®Google Scholar
• Roman MC, Minton-Summers S. 1998. Assessment of biofilm formation in the International Space Station Water Recovery and Management system. Life Support Biosph Sci. 5:45–51.
   PubMedGoogle Scholar
• Santomartino R, Waajen AC, de Wit W, Nicholson N, Parmitano L, Loudon CM, Moeller R, Rettberg P, Fuchs FM, Van Houdt R, et al. 2020. No effect of microgravity and simulated mars gravity on final bacterial cell concentrations on the international space station: applications to space bioproduction. Front Microbiol. 11:579156. doi:10.3389/fmicb.2020.579156
   PubMed Web of Science ®Google Scholar
• Sawyer DT. 1964. Metal-gluconate complexes. Chem Rev. 64:633–643. doi:10.1021/cr60232a003
   Web of Science ®Google Scholar
• Schultz JR, Taylor RD, Flanagan DT, Carr SE, Bruce RJ, Svoboda JV, Huls MH, Sauer RL, Pierson DL. 1991. Biofilm formation and control in a simulated spacecraft water system: two-year results. SAE Trans. 100:1056–1066.
   Google Scholar
• Shelobolina ES, Walker DK, Parker AE, Lust DV, Schultz JM, Dickerman GE. 2018. Inactivation of Pseudomonas aeruginosa biofilms formed under high shear stress on various hydrophilic and hydrophobic surfaces by a continuous flow of ozonated water. Biofouling. 34:826–834. doi:10.1080/08927014.2018.1506023
   PubMed Web of Science ®Google Scholar
• Sheng X, Ting YP, Pehkonen SO. 2008. The influence of ionic strength, nutrients and pH on bacterial adhesion to metals. J Colloid Interface Sci. 321:256–264. doi:10.1016/j.jcis.2008.02.038
   PubMed Web of Science ®Google Scholar
• Siems K, Müller DW, Maertens L, Ahmed A, Van Houdt R, Mancinelli RL, Baur S, Brix K, Kautenburger R, Caplin N, et al. 2022. Testing laser-structured antimicrobial surfaces under space conditions: the design of the ISS experiment BIOFILMS. Front Space Technol. 2:773244. doi:10.3389/frspt.2021.773244
   Google Scholar
• Sinde E, Carballo J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiol. 17:439–447.
   Web of Science ®Google Scholar
• Squire MD, Rotter HA, Lee J, Packham N, Brady TK, Kelly R, Ott CM. 2014. International Space Station (ISS) Orbital Replaceable Unit (ORU) Wet Storage Risk Assessment. NASA.
   Google Scholar
• Stoodley P, Sauer K, Davies DG, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu Rev Microbiol. 56:187–209. doi:10.1146/annurev.micro.56.012302.160705
   PubMed Web of Science ®Google Scholar
• Thompson AF, English EL, Nock AM, Willsey GG, Eckstrom K, Cairns B, Bavelock M, Tighe SW, Foote A, Shulman H, et al. 2020. Characterizing species interactions that contribute to biofilm formation in a multispecies model of a potable water bacterial community. Microbiology (Reading). 166:34–43. doi:10.1099/mic.0.000849
   PubMed Web of Science ®Google Scholar
• Van Houdt R, Leys N. 2020. Monitoring the microbial burden in manned space stations. In: Choukèr A, editor. Stress challenges and immunity in space: from mechanisms to monitoring and preventive strategies. Cham: Springer, p. 463–475. doi:10.1007/978-3-030-16996-1_25
   Google Scholar
• Van Houdt R, Michiels CW. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. J Appl Microbiol. 109:1117–1131. doi:10.1111/j.1365-2672.2010.04756.x
   PubMed Web of Science ®Google Scholar
• Van Houdt R, Vandecraen J, Leys N, Monsieurs P, Aertsen A. 2021. Adaptation of Cupriavidus metallidurans CH34 to toxic zinc concentrations involves an uncharacterized ABC-type transporter. Microorganisms. 9:309. doi:10.3390/microorganisms9020309
   PubMed Web of Science ®Google Scholar
• Walker SL. 2005. The role of nutrient presence on the adhesion kinetics of Burkholderia cepacia G4g and ENV435g. Colloids Surf B Biointerfaces. 45:181–188. doi:10.1016/j.colsurfb.2005.08.007
   PubMed Web of Science ®Google Scholar
• Wang D, Jia R, Kumseranee S, Punpruk S, Gu TY. 2021. Comparison of 304 and 316 stainless steel microbiologically influenced corrosion by an anaerobic oilfield biofilm consortium. Eng Failure Anal. 122:105275. doi:10.1016/j.engfailanal.2021.105275.
   Web of Science ®Google Scholar
• Wang A, Jones IP, Landini G, Mei J, Tse YY, Li YX, Ke L, Huang Y, Liu LI, Wang C, et al. 2018. Backscattered electron imaging and electron backscattered diffraction in the study of bacterial attachment to titanium alloy structure. J Microsc. 270:53–63. doi:10.1111/jmi.12649
   PubMed Web of Science ®Google Scholar
• Wang S, Liu X, Liu H, Zhang L, Guo Y, Yu S, Wozniak DJ, Ma LZ. 2015. The exopolysaccharide Psl-eDNA interaction enables the formation of a biofilm skeleton in Pseudomonas aeruginosa. Environ Microbiol Rep. 7:330–340. doi:10.1111/1758-2229.12252
   PubMed Web of Science ®Google Scholar
• Wieland PO, Center G. 1998. Living together in space: the design and operation of the life support systems on the International Space Station. National Aeronautics and Space Administration, Marshall Space Flight Center.
   Google Scholar
• Yang J, Barrila J, Mark Ott C, King O, Bruce R, McLean RJC, Nickerson CA. 2021. Longitudinal characterization of multispecies microbial populations recovered from spaceflight potable water. NPJ Biofilms Microbiomes. 7:70. doi:10.1038/s41522-021-00240-5
   PubMed Web of Science ®Google Scholar
• Zea L, McLean RJC, Rook TA, Angle G, Carter DL, Delegard A, Denvir A, Gerlach R, Gorti S, McIlwaine D, et al. 2020. Potential biofilm control strategies for extended spaceflight missions. Biofilm. 2:100026. doi:10.1016/j.bioflm.2020.100026
   PubMedGoogle Scholar
• Zhang M, Chen S, Gnegy M, Ye C, Lin W, Lin H, Yu X. 2018. Environmental strains potentially contribute to the proliferation and maintenance of antibiotic resistance in drinking water: a case study of Cupriavidus metallidurans. Sci Total Environ. 643:819–826. doi:10.1016/j.scitotenv.2018.06.013
   PubMed Web of Science ®Google Scholar
• Zheng S, Bawazir M, Dhall A, Kim HE, He L, Heo J, Hwang G. 2021. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front Bioeng Biotechnol. 9:643722. doi:10.3389/fbioe.2021.643722
   PubMed Web of Science ®Google Scholar
• Zhou S, Schoneich C, Singh SK. 2011. Biologics formulation factors affecting metal leachables from stainless steel. AAPS PharmSciTech. 12:411–421. doi:10.1208/s12249-011-9592-3
   PubMed Web of Science ®Google Scholar