Skip to main content
Log in

Proton transfer reaction–mass spectrometry: online and rapid determination of volatile organic compounds of microbial origin

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Analytical tools for the identification and quantification of volatile organic compounds (VOCs) produced by microbial cultures have countless applications in an industrial and research context which are still not fully exploited. The various techniques for VOC analysis generally arise from the application of different scientific and technological philosophies, favoring either sample throughput or chemical information. Proton transfer reaction–mass spectrometry (PTR-MS) represents a valid compromise between the two aforementioned approaches, providing rapid and direct measurements along with highly informative analytical output. The present paper reviews the main applications of PTR-MS in the microbiological field, comprising food, environmental, and medical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abanda-Nkpwatt D, Musch M, Tschiersch J, Boettner M, Schwab W (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57:4025–4032

    Article  CAS  PubMed  Google Scholar 

  • Bäck J, Aaltonen H, Hellén H, Kajos MK, Patokoski J, Taipale R, Pumpanen J, Heinonsalo J (2010) Variable emissions of microbial volatile organic compounds (MVOCs) from root-associated fungi isolated from Scots pine. Atmos Environ 44:3651–3659

    Article  Google Scholar 

  • Blake RS, Whyte C, Hughes CO, Ellis AM, Monks PS (2004) Demonstration of proton-transfer reaction time-of-flight mass spectrometry for real-time analysis of trace volatile organic compounds. Anal Chem 76:3841–3845

    Article  CAS  Google Scholar 

  • Blasioli S, Biondi E, Samudrala D, Spinelli F, Cellini A, Bertaccini A, Cristescu SM, Braschi I (2014) Identification of volatile markers in potato brown rot and ring rot by combined GC-MS and PTR-MS techniques: study on in vitro and in vivo samples. J Agr Food Chem 62:337–347

    Article  CAS  Google Scholar 

  • Borneman AR, Schmidt SA, Pretorius IS (2013) At the cutting-edge of grape and wine biotechnology. Trends Genet 29:263–271

    Article  CAS  PubMed  Google Scholar 

  • Braden B, Lembcke B, Kuker W, Caspary WF (2007) 13C-breath tests: current state of the art and future directions. Dig Liver Dis 39:795–805

    Article  CAS  PubMed  Google Scholar 

  • Bunge M, Araghipour N, Mikoviny T, Dunkl J, Schnitzhofer R, Hansel A, Schinner F, Wisthaler A, Margesin R, Mark TD (2008) On-line monitoring of microbial volatile metabolites by proton transfer reaction-mass spectrometry. Appl Environ Microbiol 74:2179–2186

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Capozzi V, Spano G (2011) Food microbial biodiversity and “Microbes of Protected Origin”. Front Microbiol 2:237

    Article  PubMed Central  PubMed  Google Scholar 

  • Capozzi V, Russo P, Beneduce L, Weidmann S, Grieco F, Guzzo J, Spano G (2010) Technological properties of Oenococcus oeni strains isolated from typical southern Italian wines. Lett Appl Microbiol 50:327–334

    Article  CAS  PubMed  Google Scholar 

  • Crespo E, Cristescu SM, de Ronde H, Kuijper S, Kolk AHJ, Anthony RM, Harren FJM (2011) Proton transfer reaction mass spectrometry detects rapid changes in volatile metabolite emission by Mycobacterium smegmatis after the addition of specific antimicrobial agents. J Microbiol Methods 86:8–15

    Article  CAS  PubMed  Google Scholar 

  • Critchley A, Elliott TS, Harrison G, Mayhew CA, Thompson JM, Worthington T (2004) The proton transfer reaction mass spectrometer and its use in medical science: applications to drug assays and the monitoring of bacteria. Int J Mass Spectrom 239:235–241

    Article  CAS  Google Scholar 

  • Di Toro MR, Capozzi V, Beneduce L, Alexandre H, Tristezza M, Durante M, Tufariello M, Grieco F, Spano G (2015) Intraspecific biodiversity and “spoilage potential” of Brettanomyces bruxellensis in Apulian wines. LWT-Food Sci Technol 60:102–108

    Article  Google Scholar 

  • Dickschat JS, Martens T, Brinkhoff T, Simon M, Schulz S (2005) Volatiles Released by a Streptomyces Species Isolated from the North Sea. Chem Biodivers 2:837–865

    Article  CAS  PubMed  Google Scholar 

  • Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703

    Article  CAS  PubMed  Google Scholar 

  • Hansel A, Jordan A, Holzinger R, Prazeller P, Vogel W, Lindinger W (1995) Proton transfer reaction mass spectrometry: on-line trace gas analysis at the ppb level. Int J Mass Spectrom 149–150:609–619

    Article  Google Scholar 

  • Heddergott C, Calvo AM, Latgé JP (2014) The volatome of Aspergillus fumigatus. Eukaryotic Cell 13:1014–1025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jaksch D, Margesin R, Mikoviny T, Skalny JD, Hartungen E, Schinner F, Mason NJ, Märk TD (2004) The effect of ozone treatment on the microbial contamination of pork meat measured by detecting the emissions using PTR-MS and by enumeration of microorganisms. Int J Mass Spectrom 239:209–214

    Article  CAS  Google Scholar 

  • Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res 14:215–237

    Article  CAS  PubMed  Google Scholar 

  • Jordan A, Haidacher S, Hanel G, Hartungen E, Märk L, Seehauser H, Schottkowsky R, Sulzer P, Märk TD (2009) A high resolution and high sensitivity proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS). Int J Mass Spectrom 286:122–128

    Article  CAS  Google Scholar 

  • Jünger M, Vautz W, Kuhns M, Hofmann L, Ulbricht S, Baumbach JI, Quintel M, Perl T (2012) Ion mobility spectrometry for microbial volatile organic compounds: a new identification tool for human pathogenic bacteria. Appl Microbiol Biotechnol 93:2603–2614

    Article  PubMed Central  PubMed  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360

    Article  CAS  PubMed  Google Scholar 

  • Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Microbiol Biotechnol 81:1001–1012

    Article  CAS  PubMed  Google Scholar 

  • Kai M, Crespo E, Cristescu SM, Harren FJM, Francke W, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976

    Article  CAS  PubMed  Google Scholar 

  • Kim JL, Elfman L, Mi Y, Wieslander G, Smedje G, Norbäck D (2007) Indoor molds, bacteria, microbial volatile organic compounds and plasticizers in schools – associations with asthma and respiratory symptoms in pupils. Indoor Air 17:153–163

    Article  CAS  PubMed  Google Scholar 

  • Kim TG, Lee E-H, Cho K-S (2012) Effects of nonmethane volatile organic compounds on microbial community of methanotrophic biofilter. Appl Microbiol Biotechnol 97:6549–6559

    Article  PubMed  Google Scholar 

  • Korpi A, Järnberg J, Pasanen A-L (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–193

    Article  CAS  PubMed  Google Scholar 

  • Kuppusami S, Clokie MRJ, Panayi T, Ellis AM, Monks PS (2015) Metabolite profiling of Clostridium difficile ribotypes using small molecular weight volatile organic compounds. Metabolomics 11:251–260

  • Kviatkovski I, Chernin L, Yarnitzky T, Frumin I, Sobel N, Helman Y (2015) Pseudomonas aeruginosa activates the quorum sensing LuxR response regulator through secretion of 2-aminoacetophenone. Chem Commun. doi:10.1039/C4CC10393A

    Google Scholar 

  • Lemfack MC, Nickel J, Dunkel M, Preissner R, Piechulla B (2014) mVOC: a database of microbial volatiles. Nucl Acids Res 42:D744–D748

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lindinger W, Jordan A (1998) Proton-transfer-reaction mass spectrometry (PTR–MS): on-line monitoring of volatile organic compounds at pptv levels. Chem Soc Rev 27:347

    Article  CAS  Google Scholar 

  • Luchner M, Gutmann R, Bayer K, Dunkl J, Hansel A, Herbig J, Singer W, Strobl F, Winkler K, Striedner G (2012) Implementation of proton transfer reaction-mass spectrometry (PTR-MS) for advanced bioprocess monitoring. Biotechnol Bioprocess Eng 109:3059–3069

    CAS  Google Scholar 

  • Makhoul S, Romano A, Cappellin L, Spano G, Capozzi V, Benozzi E, Märk TD, Aprea E, Gasperi F, El-Nakat H, Guzzo J, Biasioli F (2014) Proton-transfer-reaction mass spectrometry for the study of the production of volatile compounds by bakery yeast starters: PTR-MS study of bakery yeast starters. J Mass Spectrom 49:850–859

    Article  CAS  PubMed  Google Scholar 

  • Mallette ND, Knighton WB, Strobel GA, Carlson RP, Peyton BM (2012) Resolution of volatile fuel compound profiles from Ascocoryne sarcoides: a comparison by proton transfer reaction-mass spectrometry and solid phase microextraction gas chromatography-mass spectrometry. AMB Express 2:23

    Article  PubMed Central  PubMed  Google Scholar 

  • Mayr D, Margesin R, Klingsbichel E, Hartungen E, Jenewein D, Schinner F, Mark TD (2003a) Rapid detection of meat spoilage by measuring volatile organic compounds by using proton transfer reaction mass spectrometry. Appl Environ Microbiol 69:4697–4705

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mayr D, Margesin R, Schinner F, Märk T (2003b) Detection of the spoiling of meat using PTR–MS. Int J Mass Spectrom 223–224:229–235

    Article  Google Scholar 

  • Mayrhofer S, Mikoviny T, Waldhuber S, Wagner AO, Innerebner G, Franke-Whittle IH, Märk TD, Hansel A, Insam H (2006) Microbial community related to volatile organic compound (VOC) emission in household biowaste. Environ Microbiol 8:1960–1974

    Article  CAS  PubMed  Google Scholar 

  • Minerdi D, Bossi S, Maffei ME, Gullino ML, Garibaldi A (2011) Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansin A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol Ecol 76:342–351

    Article  CAS  PubMed  Google Scholar 

  • Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83

    Article  Google Scholar 

  • Nawrath T, Mgode GF, Weetjens B, Kaufmann SHE, Schulz S (2012) The volatiles of pathogenic and nonpathogenic mycobacteria and related bacteria. Beilstein J Org Chem 8:290–299

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Hara M, Mayhew CA (2009) A preliminary comparison of volatile organic compounds in the headspace of cultures of Staphylococcus aureus grown in nutrient, dextrose and brain heart bovine broths measured using a proton transfer reaction mass spectrometer. J Breath Res 3:027001

    Article  PubMed  Google Scholar 

  • Özdestan Ö, van Ruth SM, Alewijn M, Koot A, Romano A, Cappellin L, Biasioli F (2013) Differentiation of specialty coffees by proton transfer reaction-mass spectrometry. Food Res Int 53:433–439

    Article  Google Scholar 

  • Pagans E, Font X, Sánchez A (2006) Emission of volatile organic compounds from composting of different solid wastes: abatement by biofiltration. J Hazard Mater 131:179–186

    Article  CAS  PubMed  Google Scholar 

  • Papurello D, Soukoulis C, Schuhfried E, Cappellin L, Gasperi F, Silvestri S, Santarelli M, Biasioli F (2012) Monitoring of volatile compound emissions during dry anaerobic digestion of the organic fraction of municipal solid waste by Proton Transfer Reaction Time-of-Flight Mass Spectrometry. Bioresour Technol 126:254–265

    Article  CAS  PubMed  Google Scholar 

  • Rabe P, Citron CA, Dickschat JS (2013) Volatile terpenes from actinomycetes: a biosynthetic study correlating chemical analyses to genome data. Chembiochem 14:2345–2354

    Article  CAS  PubMed  Google Scholar 

  • Schmidberger T, Gutmann R, Bayer K, Kronthaler J, Huber R (2014) Advanced online monitoring of cell culture off-gas using proton transfer reaction mass spectrometry. Biotechnol Progr 30:496–504

    Article  CAS  Google Scholar 

  • Schulz S, Dickschat JS (2007) Bacterial volatiles: the smell of small organisms. Nat Prod Rep 24:814–842

    Article  CAS  PubMed  Google Scholar 

  • Seewald MSA, Singer W, Knapp BA, Franke-Whittle IH, Hansel A, Insam H (2010) Substrate-induced volatile organic compound emissions from compost-amended soils. Biol Fert Soils 46:371–382

    Article  Google Scholar 

  • Silcock P, Alothman M, Zardin E, Heenan S, Siefarth C, Bremer PJ, Beauchamp J (2014) Microbially induced changes in the volatile constituents of fresh chilled pasteurised milk during storage. Food Packaging and Shelf Life 2:81–90

    Article  Google Scholar 

  • Soukoulis C, Aprea E, Biasioli F, Cappellin L, Schuhfried E, Märk TD, Gasperi F (2010) Proton transfer reaction time-of-flight mass spectrometry monitoring of the evolution of volatile compounds during lactic acid fermentation of milk. Rapid Commun Mass Spectrom 24:2127–2134

    Article  CAS  PubMed  Google Scholar 

  • Splivallo R, Ebeler SE (2015) Sulfur volatiles of microbial origin are key contributors to human-sensed truffle aroma. Appl Microbiol Biotechnol 99:2583–92

  • Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev Microbiol 4:333–382

    Article  CAS  PubMed  Google Scholar 

  • Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, Griffin M, Spakowicz D, Sears J (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154:3319–3328

    Article  CAS  PubMed  Google Scholar 

  • Sumby KM, Grbin PR, Jiranek V (2014) Implications of new research and technologies for malolactic fermentation in wine. Appl Microbiol Biotechnol 98:8111–8132

    Article  CAS  PubMed  Google Scholar 

  • Swiegers JH, Bartowsky EJ, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11:139–173

    Article  CAS  Google Scholar 

  • Tait E, Perry JD, Stanforth SP, Dean JR (2014) Bacteria detection based on the evolution of enzyme-generated volatile organic compounds: Determination of Listeria monocytogenes in milk samples. Anal Chim Acta 848:80–87

    Article  CAS  PubMed  Google Scholar 

  • Thorn RMS, Greenman J (2012) Microbial volatile compounds in health and disease conditions. J Breath Res 6:024001

    Article  PubMed  Google Scholar 

  • Tristezza M, Vetrano C, Bleve G, Spano G, Capozzi V, Logrieco A, Mita G, Grieco F (2013) Biodiversity and safety aspects of yeast strains characterized from vineyards and spontaneous fermentations in the Apulia Region, Italy. Food Microbiol 36:335–342

    Article  CAS  PubMed  Google Scholar 

  • Tsevdou M, Soukoulis C, Cappellin L, Gasperi F, Taoukis PS, Biasioli F (2013) Monitoring the effect of high pressure and transglutaminase treatment of milk on the evolution of flavour compounds during lactic acid fermentation using PTR-ToF-MS. Food Chem 138:2159–2167

    Article  CAS  PubMed  Google Scholar 

  • Weise T, Kai M, Gummesson A, Troeger A, von Reuß S, Piepenborn S, Kosterka F, Sklorz M, Zimmermann R, Francke W, Piechulla B (2012) Volatile organic compounds produced by the phytopathogenic bacterium Xanthomonas campestris pv. vesicatoria 85-10. Beilstein J Org Chem 8:579–596

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zehm S, Schweinitz S, Würzner R, Colvin HP, Rieder J (2012) Detection of Candida albicans by mass spectrometric fingerprinting. Curr Microbiol 64:271–275

    Article  CAS  PubMed  Google Scholar 

  • Zoller HF, Clark WM (1921) The production of volatile fatty acids by bacteria of the dysentery group. J Gen Physiol 3:325–330

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Spano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 712 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romano, A., Capozzi, V., Spano, G. et al. Proton transfer reaction–mass spectrometry: online and rapid determination of volatile organic compounds of microbial origin. Appl Microbiol Biotechnol 99, 3787–3795 (2015). https://doi.org/10.1007/s00253-015-6528-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6528-y

Keywords

Navigation