Applied Microbiology and Biotechnology

, Volume 102, Issue 19, pp 8525–8536 | Cite as

Adhesion of Rhodococcus ruber IEGM 342 to polystyrene studied using contact and non-contact temperature measurement techniques

  • Anastasiia V. KrivoruchkoEmail author
  • Anastasia Yu Iziumova
  • Maria S. Kuyukina
  • Oleg A. Plekhov
  • Oleg B. Naimark
  • Irina B. Ivshina
Methods and protocols


Adhesion of industrially important bacteria to solid carriers through the example of actinobacterium Rhodococcus ruber IEGM 342 adhered to polystyrene was studied using real-time methods, such as infrared (IR) thermography and thermometry with platinum resistance (PR) detectors. Dynamics of heat rate and heat production was determined at early (within first 80 min) stages of rhodococcal cell adhesion. Heat rate was maximal (1.8 × 10−3–2.7 × 10−3 W) at the moment of cell loading. Heat production was detected for the entire length of adhesion, and its dynamics depended on concentration of rhodococcal cells. At high (1 × 1010 CFU/ml) cell concentration, a stimulative (in 1.7 and 1.4 times consequently) effect of polystyrene treatment with Rhodococcus-biosurfactant on the number of adhered rhodococcal cells and cumulative heat production at rhodococcal cell adhesion was revealed. The values of heat flows (heat rate 0.3 × 10−3–2.7 × 10−3 W, heat production up to 8.2 × 10−3 J, and cumulative heat production 0.20–0.53 J) were 530 times higher than those published elsewhere that indicated high adhesive activity of R. ruber IEGM 342 towards polystyrene. To analyze experimental results and predict effects of boundary conditions on the temperature distribution, a mathematical model for heating a polystyrene microplate with distributed heat sources has been developed. Two independent experimental methods and the numerical modeling make it possible to verify the experimental results and to propose both contact and non-contact techniques for analyzing kinetics of bacterial adhesion.


Bacterial adhesion Adhesion thermodynamics Infrared thermography Platinum resistance thermometers Rhodococcus actinobacteria 


Funding information

This work was performed as part of the State Tasks 6.3330.2017/4.6, 116012010212, and the State Registration Theme No. 01201353247 from the RF Ministry of Science and Higher Education.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2018_9297_MOESM1_ESM.pdf (219 kb)
ESM 1 (PDF 219 kb)


  1. Absolom DR, Lamberti FV, Policova Z, Zingg W, van Oss CJ, Neumann AW (1983) Surface thermodynamics of bacterial adhesion. Appl Environ Microbiol 46:90–97PubMedPubMedCentralGoogle Scholar
  2. Adamczyk Z, Siwek B, Zembala M, Weroński P (1992) Kinetics of localized adsorption of colloid particles. Langmuir 8:2605–2610CrossRefGoogle Scholar
  3. Adamczyk Z, Siwek B, Zembala M, Belouschek P (1994) Kinetics of localized adsorption of colloid particles. Adv Colloid Interf Sci 48:151–280CrossRefGoogle Scholar
  4. Adamczyk Z, Jaszczółt K, Siwek B (2005) Irreversible adsorption of colloid particles on heterogeneous surfaces. Appl Surf Sci 252:723–729. CrossRefGoogle Scholar
  5. Andrews CS, Denyer SP, Hall B, Hanlon GW, Lloyd AW (2001) A comparison of the use of an ATP-based bioluminescent assay and image analysis for the assessment of bacterial adhesion to standard HEMA and biomimetic soft contact lenses. Biomaterials 22:3225–3233. CrossRefPubMedGoogle Scholar
  6. Astasov-Frauenhoffer M, Braissant O, Hauser-Gerspach I, Daniels AU, Wirz D, Weiger R, Waltimo T (2011) Quantification of vital adherent Streptococcus sanguinis cells on protein-coated titanium after disinfectant treatment. J Mater Sci Mater Med 22:2045–2051. CrossRefPubMedGoogle Scholar
  7. Bale JS, O’Doherty R, Atkinson HJ, Stevenson RA (1984) An automatic thermoelectric cooling method and computer-based recording system for supercooling point studies on small invertebrates. Cryobiology 21:340–347. CrossRefGoogle Scholar
  8. Bayoudh S, Othmane A, Mora L, Ben OH (2009) Assessing bacterial adhesion using DLVO and XDLVO theories and the jet impingement technique. Colloids Surf B: Biointerfaces 73:1–9. CrossRefPubMedGoogle Scholar
  9. Bos R, van der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions—its mechanisms and methods for study. FEMS Microbiol Rev 23:179–229. CrossRefPubMedGoogle Scholar
  10. Bouderbala K, Nouira H, Girault M, Videcoq E (2016) Experimental thermal regulation of an ultra-high precision metrology system by combining modal identification method and model predictive control. Appl Therm Eng 104:504–515. CrossRefGoogle Scholar
  11. Braissant O, Wirz D, Göpfert B, Daniels AU (2010) Use of isothermal microcalorimetry to monitor microbial activities. FEMS Microbiol Lett 303:1–8. CrossRefPubMedGoogle Scholar
  12. Bravo D, Braissant O, Solokhina A, Clerc M, Daniels AU, Verrecchia E, Junier P (2011) Use of an isothermal microcalorimetry assay to characterize microbial oxalotrophic activity. FEMS Microbiol Ecol 78:266–274. CrossRefPubMedGoogle Scholar
  13. Chen G, Rockhold M, Strevett KA (2003) Equilibrium and kinetic adsorption of bacteria on alluvial sand and surface thermodynamic interpretation. Res Microbiol 154:175–181. CrossRefPubMedGoogle Scholar
  14. Chizzotti ML, Heiderich D, Aziani WLB, Ladeira MM, Valente EEL, Yanagi Junior T, Chizzotti FHM, Schiassi L, Lourençoni D (2013) Protein turnover and infrared thermography in Nellore bulls classified for residual feed intake. In: Oltjen JW (ed) Energy and protein metabolism and nutrition is sustainable animal protection. Wageningen Academic Publishers, Wageningen, pp 125–126CrossRefGoogle Scholar
  15. de Carvalho CCCR, Costa SS, Fernandes P, Couto I, Viveiros M (2014) Membrane transport systems and the biodegradation potential and pathogenicity of genus Rhodococcus. Front Physiol 5:1–13. CrossRefGoogle Scholar
  16. Diao M, Taran E, Mahler S, Nguyen TAH, Nguyen AV (2014) Quantifying adhesion of acidophilic bioleaching bacteria to silica and pyrite by atomic force microscopy with a bacterial probe. Colloids Surf B: Biointerfaces 115:229–236. CrossRefPubMedGoogle Scholar
  17. Dinamarca MA, Orellana L, Aguirre J, Baeza P, Espinoza G, Canales C, Ojeda J (2014) Biodesulfurization of dibenzothiophene and gas oil using a bioreactor containing a catalytic bed with Rhodococcus rhodochrous immobilized on silica. Biotechnol Lett 36:1649–1652. CrossRefGoogle Scholar
  18. Fatile IA (1985) Rheological behaviour of concentrated yeast suspension. J Chem Technol Biotechnol 35B:94–100CrossRefGoogle Scholar
  19. Gallardo-Moreno AM, González-Martín ML, Pérez-Giraldo C, Garduño E, Bruque JM, Gómez-García AC (2002) Thermodynamic analysis of growth temperature dependence in the adhesion of Candida parapsilosis to polystyrene. Appl Environ Microbiol 68:2610–2613. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hauser-Gerspach I, De Freitas PS, Daniels AUD, Meyer J (2008) Adhesion of Streptococcus sanguinis to glass surfaces measured by isothermal microcalorimetry (IMC). J Biomed Mater Res B Appl Biomater 85:42–49. CrossRefGoogle Scholar
  21. Hori K, Matsumoto S (2010) Bacterial adhesion: from mechanism to control. Biochem Eng J 48:424–434. CrossRefGoogle Scholar
  22. Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517–2528. CrossRefPubMedGoogle Scholar
  23. Hunt VL, Lock GD, Pickering SG, Charnley AK (2011) Application of infrared thermography to the study of behavioural fever in the desert locust. J Therm Biol 36:443–451. CrossRefGoogle Scholar
  24. Ivshina IB, Kuyukina MS, Krivoruchko AV, Plekhov OA, Naimark OB, Podorozhko EA, Lozinsky VI (2013) Biosurfactant-enhanced immobilization of hydrocarbon-oxidizing Rhodococcus ruber on sawdust. Appl Microbiol Biotechnol 97:5315–5327. CrossRefPubMedGoogle Scholar
  25. Iziumova A, Vshivkov A, Prokhorov A, Kostina A, Plekhov O (2016) The study of energy balance in metals under deformation and failure process. Quant Infrared Thermography J 13:242–256. CrossRefGoogle Scholar
  26. Jacobs A, Lafolie F, Herry JM, Debroux M (2007) Kinetic adhesion of bacterial cells to sand: cell surface properties and adhesion rate. Colloids Surf B: Biointerfaces 59:35–45. CrossRefPubMedGoogle Scholar
  27. Khan MMT, Ista LK, Lopez GP, Schuler AJ (2011) Experimental and theoretical examination of surface energy and adhesion of nitrifying and heterotrophic bacteria using self-assembled monolayers. Environ Sci Technol 45:1055–1060. CrossRefPubMedGoogle Scholar
  28. Kinnby B, Chávez de Paz LE (2016) Plasminogen coating increases initial adhesion of oral bacteria in vitro. Microb Pathog 100:10–16. CrossRefPubMedGoogle Scholar
  29. Kluge B, Peters A, Krüger J, Wessolek G (2013) Detection of soil microbial activity by infrared thermography (IRT). Soil Biol Biochem 57:383–389. CrossRefGoogle Scholar
  30. Kuyukina MS, Ivshina IB, Philp JC, Christofi N, Dunbar SA, Ritchkova MI (2001) Recovery of Rhodococcus biosurfactants using methyl tertiary-butyl ether extraction. J Microbiol Methods 46:149–156. CrossRefPubMedGoogle Scholar
  31. Kuyukina MS, Ivshina IB, Osipenko MA, Nyashin YI, Tyulenyova AN, Serebrennikova MK, Krivoruchko AV (2007) A kinetic model of bacterial cell immobilization process on the solid carrier. Russ J Biomech 11:76–84Google Scholar
  32. Kuyukina MS, Ivshina IB, Baeva TA, Kochina OA, Gein SV, Chereshnev VA (2015) Trehalolipid biosurfactants from nonpathogenic Rhodococcus actinobacteria with diverse immunomodulatory activities. New Biotechnol 32:559–568. CrossRefGoogle Scholar
  33. Kuyukina MS, Ivshina IB, Serebrennikova MK, Krivoruchko AV, Korshunova IO, Peshkur TA, Cunningham CJ (2017) Oilfield wastewater biotreatment in a fluidized-bed bioreactor using co-immobilized Rhodococcus cultures. J Environ Chem Eng 5:1252–1260. CrossRefGoogle Scholar
  34. Kwak BS, Kim HJ, Kim HO, Jung H II (2010) An integrated photo-thermal sensing system for rapid and direct diagnosis of anemia. Biosens Bioelectron 26:1679–1683. CrossRefPubMedGoogle Scholar
  35. Kwak BS, Kim HO, Kim JH, Lee S, Jung H II (2012) Quantitative analysis of sialic acid on erythrocyte membranes using a photothermal biosensor. Biosens Bioelectron 35:484–488. CrossRefPubMedGoogle Scholar
  36. Lahiri BB, Divya MP, Bagavathiappan S, Thomas S, Philip J (2012) Detection of pathogenic gram negative bacteria using infrared thermography. Infrared Phys Technol 55:485–490. CrossRefGoogle Scholar
  37. Liu Y (1995) Adhesion kinetics of nitrifying bacteria on various thermoplastic supports. Colloids Surf B: Biointerfaces 5:213–219. CrossRefGoogle Scholar
  38. Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177. CrossRefPubMedGoogle Scholar
  39. Michalski L, Eckersdorf K, Kucharski J, McGhee J (2001) Temperature measurement, 2nd edn. John Wiley & Sons, Ltd, ChichesterCrossRefGoogle Scholar
  40. Morimoto E, Hirako S, Yamasaki H, Izumi M (2013) Development of on-the-go soil sensor for rice transplanter. Eng Agric Environ Food 6:141–146. CrossRefGoogle Scholar
  41. Ng EYK (2009) A review of thermography as promising non-invasive detection modality for breast tumor. Int J Therm Sci 48:849–859. CrossRefGoogle Scholar
  42. Omarova EO, Lobakova ES, Dolnikova GA, Nekrasova VV, Idiatulov RK, Kashcheeva PB, Perevertailo NG, Dedov AG (2012) Immobilization of bacteria on polymer matrices for degradation of crude oil and oil products. Mosc Univ Biol Sci Bull 67:24–30. CrossRefGoogle Scholar
  43. Pegg DE, Hayes AR (1970) A platinum resistance thermometer for use in cryobiology. Phys Med Biol 15:409–416. CrossRefPubMedGoogle Scholar
  44. Qu W, Busscher HJ, Hooymans JMM, van der Mei HC (2011) Surface thermodynamics and adhesion forces governing bacterial transmission in contact lens related microbial keratitis. J Colloid Interface Sci 358:430–436. CrossRefPubMedGoogle Scholar
  45. Ring EFJ, Ammer K (2012) Infrared thermal imaging in medicine. Physiol Meas 33:R33–R46. CrossRefPubMedGoogle Scholar
  46. Robledo-Ortíz JR, Ramírez-Arreola DE, Gomez C, González-Reynoso O, González-Núñez R (2010) Bacterial immobilization by adhesion onto agave-fiber/polymer foamed composites. Bioresour Technol 101:1293–1299. CrossRefPubMedGoogle Scholar
  47. Rochex A, Lecouturier D, Pezron I, Lebeault JM (2004) Adhesion of a Pseudomonas putida strain isolated from a paper machine to cellulose fibres. Appl Microbiol Biotechnol 65:727–733. CrossRefPubMedGoogle Scholar
  48. Sadat S, Meyhofer E, Reddy P (2012) High resolution resistive thermometry for micro/nanoscale measurements. Rev Sci Instrum 83:84902-1–84902–14. CrossRefGoogle Scholar
  49. Salaimeh AA, Campion JJ, Gharaibeh BY, Evans ME, Saito K (2011) Real-time quantification of viable bacteria in liquid medium using infrared thermography. Infrared Phys Technol 54:517–524. CrossRefGoogle Scholar
  50. Salaimeh AA, Campion JJ, Gharaibeh BY, Evans ME, Saito K (2012) Real-time quantification of Staphylococcus aureus in liquid medium using infrared thermography. Infrared Phys Technol 55:170–172. CrossRefGoogle Scholar
  51. Suttinun O, Müller R, Luepromchai E (2010) Cometabolic degradation of trichloroethene by Rhodococcus sp. strain L4 immobilized on plant materials rich in essential oils. Appl Environ Microbiol 76:4684–4690. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Tabata K, Hida F, Kiriyama T, Ishizaki N, Kamachi T, Okura I (2013) Measurement of soil bacterial colony temperatures and isolation of a high heat-producing bacterium. BMC Microbiol 13:56. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tabbagh A, Cheviron B, Henine H, Guérin R, Bechkit MA (2017) Numerical determination of vertical water flux based on soil temperature profiles. Adv Water Resour 105:217–226. CrossRefGoogle Scholar
  54. Toda K, Furuse H, Amari T, Wei X (1998) Cell concentration dependence of dynamic viscoelasticity of Escherichia coli culture suspensions. J Ferment Bioeng 85:410–415. CrossRefGoogle Scholar
  55. Usamentiaga R, Venegas P, Guerediaga J, Vega L, Molleda J, Bulnes F (2014) Infrared thermography for temperature measurement and non-destructive testing. Sensors 14:12305–12348. CrossRefPubMedGoogle Scholar
  56. Vollmer M, Möllmann K-P (2010) Microsystems. In: Infrared thermal imaging. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 445–475Google Scholar
  57. Yam KC, van der Geize R, Eltis LD (2010) Catabolism of aromatic compounds and steroids by Rhodococcus. In: Alvarez HM (ed) Biology of Rhodococcus. Springer-Verlag, Berlin Heidelberg, pp 133–169CrossRefGoogle Scholar
  58. Ye J, Shao C, Zhang X, Guo X, Gao P, Cen Y, Ma S, Liu Y (2017) Effects of DNase I coating of titanium on bacteria adhesion and biofilm formation. Mater Sci Eng C 78:738–747. CrossRefGoogle Scholar
  59. Zhong R, Pan X, Jiang L, Dai Z, Qin J, Lin B (2009) Simply and reliably integrating micro heaters/sensors in a monolithic PCR-CE microfluidic genetic analysis system. Electrophoresis 30:1297–1305. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Ecology and Genetics of MicroorganismsPermRussia
  2. 2.Perm State UniversityPermRussia
  3. 3.Institute of Continuous Media MechanicsPermRussia

Personalised recommendations