Cited by 37Microbial bioremediation and biosurfactantsMicrobial Metabolic Engineering and BioproductionSurfactants and Colloidal Systems

Towards the Anaerobic Production of Surfactin Using Bacillus subtilis

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Hoffmann, Mareen, Fernandez Cano Luna, Diana Stephanie, Xiao, Shengbin, Stegemüller, Lars, Rief, Katharina, Heravi, Kambiz Morabbi, Lilge, Lars, Henkel, Marius +1 more·2020·Frontiers in Bioengineering and Biotechnology

Abstract

The anaerobic growth of B. subtilis to synthesize surfactin poses an alternative strategy to conventional aerobic cultivations. In general, the strong foam formation observed during aerobic processes represents a major obstacle. Anaerobic processes have, amongst others, the distinct advantage that the total bioreactor volume can be exploited as foaming does not occur. Recent studies also reported on promising product per biomass yields. However, anaerobic growth in comparison to aerobic processes has several disadvantages. For example, the overall titers are comparably low and cultivations are time-consuming due to low growth rates. B. subtilis JABs24, a derivate of strain 168 with the ability to synthesize surfactin, was used as model strain in this study. Ammonium and nitrite were hypothesized to negatively influence anaerobic growth. Ammonium with initial concentrations up to 0.2 mol/L was shown to have no significant impact on growth, but increasing concentrations resulted in decreased surfactin titers and reduced nitrate reductase expression. Anaerobic cultivations spiked with increasing nitrite concentrations resulted in prolonged lag-phases. Indeed, growth rates were in a similar range after the lag-phase indicating that nitrite has a neglectable effect on the observed decreasing growth rates. In bioreactor cultivations, the specific growth rate decreased with increasing glucose concentrations during the time course of both batch and fed-batch processes to less than 0.05 1/h. In addition, surfactin titers, overall YP/X and YP/S were 53%, ∼42%, and ∼57% lower than in serum flask with 0.190 g/L, 0.344 g/g and 0.015 g/g. The YX/S, on the contrary, was 30% lower in the serum flask with 0.044 g/g. The productivities q were similar with ∼0.005 g/(g⋅h). However, acetate strongly accumulated during cultivation and was posed as further metabolite that might negatively influence anaerobic growth. Acetate added to anaerobic cultivations in a range from 0 g/L up to 10 g/L resulted in a reduced maximum and overall growth rate μ by 44% and 30%, respectively. To conclude, acetate was identified as a promising target for future process enhancement and strain engineering. Though, the current study demonstrates that the anaerobic cultivation to synthesize surfactin represents a reasonable perspective and feasible alternative to conventional processes.

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  1. Altenbuchner J. Viell P. Pelletier I. (1992). Positive selection vectors based on palindromic Dna sequences Methods Enzymol. 216 457– 466. 10.1016/0076-6879(92)16042-I 1479915 · DOI
  2. Carvalho A. L. U. de Oliveira F. H. P. C. de Mariano R. de L. R. Gouveia E. R. Souto-Maior A. M. (2010). Growth, sporulation and production of bioactive compounds by Bacillus subtilis R14. Braz. Archiv. Biol. Technol. 53 643– 652. 10.1590/S1516-89132010000300020 · DOI · Paper page
  3. Chen C.-Y. Baker S. C. Darton R. C. (2006). Batch production of biosurfactant with foam fractionation. J. Chem. Technol. Biotechnol. 81 1923– 1931. 10.1002/jctb.1625 · DOI
  4. Chtioui O. Dimitrov K. Gancel F. Dhulster P. Nikov I. (2012). Rotating discs bioreactor, a new tool for lipopeptides production. Process Biochem. 47 2020– 2024. 10.1016/j.procbio.2012.07.013 · DOI
  5. Clements L. D. Miller B. S. Streips U. N. (2002a). Comparative growth analysis of the facultative anaerobes Bacillus subtilis, Bacillus licheniformis, and Escherichia coli. Syst. Appl. Microbiol. 25 284– 286. 10.1078/0723-2020-00108 12353884 · DOI
  6. Clements L. D. Streips U. N. Miller B. S. (2002b). Differential proteomic analysis of Bacillus subtilis nitrate respiration and fermentation in defined medium. Proteomics 2: 11. 12469342
  7. Cooper D. G. Macdonald C. R. Duff S. J. B. Kosaric N. (1981). Enhanced production of surfactin from Bacillus subtilis by continuous product removal and metal cation additions. Appl. Environ. Microbiol. 42 408– 412. 10.1128/AEM.42.3.408-412.1981 16345840 PMC244028 · DOI · Paper page
  8. Coutte F. Lecouturier D. Ait Yahia S. Leclère V. Béchet M. Jacques P. (2010). Production of surfactin and fengycin by Bacillus subtilis in a bubbleless membrane bioreactor. Appl. Microbiolo. Biotechnol. 87 499– 507. 10.1007/s00253-010-2504-2508 20221757 · DOI
  9. Coutte F. Lecouturier D. Dimitrov K. Guez J.-S. Delvigne F. Dhulster P. (2017). Microbial lipopeptide production and purification bioprocesses, current progress and future challenges. Biotechnol. J. 12: 1600566. 10.1002/biot.201600566 28636078 · DOI
  10. Cruz Ramos H. Boursier L. Moszer I. Kunst F. Danchin A. Glaser P. (1995). Anaerobic transcription activation in Bacillus subtilis: identification of distinct FNR-dependent and -independent regulatory mechanisms. EMBO J. 14 5984– 5994. 10.1002/j.1460-2075.1995.tb00287.x 8846791 PMC394718 · DOI
  11. Cruz Ramos H. Hoffmann T. Marino M. Nedjari H. Presecan-Siedel E. Dreesen O. (2000). Fermentative metabolism of Bacillus subtilis: physiology and regulation of gene expression. J. Bacteriol. 182 3072– 3080. 10.1128/JB.182.11.3072-3080.2000 10809684 PMC94491 · DOI
  12. Davis D. A. Lynch H. C. Varley J. (1999). The production of Surfactin in batch culture by Bacillus subtilis ATCC 21332 is strongly influenced by the conditions of nitrogen metabolism. Enzyme Microb. Technol. 25 322– 329. 10.1016/S0141-0229(99)00048-4 · DOI
  13. Davis D. A. Lynch H. C. Varley J. (2001). The application of foaming for the recovery of surfactin from B. subtilis ATCC 21332 cultures. Enzyme Microb. Technol. 28 346– 354. 10.1016/S0141-0229(00)00327-6 11240190 · DOI
  14. Espinosa-de-los-Monteros J. Martinez A. Valle F. (2001). Metabolic profiles and aprE expression in anaerobic cultures of Bacillus subtilis using nitrate as terminal electron acceptor. Appl. Microbiol. Biotechnol. 57 379– 384. 10.1007/s002530100749 11759689 · DOI
  15. Geissler M. Heravi K. M. Henkel M. Hausmann R. (2019a). “Lipopeptide biosurfactants from Bacillus Species,” in Biobased Surfactants, eds Hayes D. G. Solaiman D. K. Y. Ashby R. D. (Amsterdam: Elsevier), 205– 240. 10.1016/B978-0-12-812705-6.00006-X · DOI
  16. Geissler M. Kühle I. Morabbi Heravi K. Altenbuchner J. Henkel M. Hausmann R. (2019b). Evaluation of surfactin synthesis in a genome reduced Bacillus subtilis strain. AMB Express 9: 84. 10.1186/s13568-019-0806-5 31190306 PMC6562014 · DOI · Paper page
  17. Geissler M. Oellig C. Moss K. Schwack W. Henkel M. Hausmann R. (2017). High-performance thin-layer chromatography (HPTLC) for the simultaneous quantification of the cyclic lipopeptides Surfactin, Iturin A and Fengycin in culture samples of Bacillus species. J. Chromatogr. B 1044–1045 214– 224. 10.1016/j.jchromb.2016.11.013 28153674 · DOI · Paper page
  18. Härtig E. Jahn D. (2012). “Regulation of the anaerobic metabolism in Bacillus subtilis. Adv. Microb. Physiol. 61 195– 216. 10.1016/B978-0-12-394423-8.00005-6 23046954 · DOI
  19. Henkel M. Geissler M. Weggenmann F. Hausmann R. (2017). Production of microbial biosurfactants: status quo of rhamnolipid and surfactin towards large-scale production. Biotechnol. J. 12: 1600561. 10.1002/biot.201600561 28544628 · DOI
  20. Hoffmann T. Frankenberg N. Marino M. Jahn D. (1998). Ammonification in Bacillus subtilis utilizing dissimilatory nitrite reductase is dependent onresDE. J. Bacteriol. 180 186– 189. 10.1128/JB.180.1.186-189.1998 9422613 PMC106869 · DOI
  21. Javaheri M. Jenneman G. E. McInerney M. J. Knapp R. M. (1985). Anaerobic production of a biosurfactant by Bacillus licheniformis JF-2. Appl. Environ. Microbiol. 50 698– 700. 10.1128/AEM.50.3.698-700.1985 16346889 PMC238693 · DOI
  22. Javed M. Baghaei-Yazdi N. (2016). Nutritional optimization for anaerobic growth of Bacillus steaothermophilus LLD-16. J. Rad. Res. Appl. Sci. 9 170– 179. 10.1016/j.jrras.2015.12.007 · DOI
  23. Killam R. L. Barenfanger J. Cox M. (2003). Influence of lack of CO2 on anaerobic bacteria: a quick method to verify the absence of CO2. J. Clin. Microbiol. 41 2201– 2202. 10.1128/JCM.41.5.2201-2002.2003 12734279 PMC154685 · DOI
  24. Lasko D. R. Zamboni N. Sauer U. (2000). Bacterial response to acetate challenge: a comparison of tolerance among species. Appl. Microbiol. Biotechnol. 54 243– 247. 10.1007/s002530000339 10968640 · DOI
  25. Leejeerajumnean A. Ames J. M. Owens J. D. (2000). Effect of ammonia on the growth of Bacillus species and some other bacteria. Lett. Appl. Microbiol. 30 385– 389. 10.1046/j.1472-765x.2000.00734.x 10792668 · DOI
  26. Li Y. Héloir M. Zhang X. Geissler M. Trouvelot S. Jacquens L. (2019). Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defence stimulation. Mol. Plant Pathol. 20 1037– 1050. 10.1111/mpp.12809 31104350 PMC6640177 · DOI
  27. Marino M. Ramos H. C. Hoffmann T. Glaser P. Jahn D. (2001). Modulation of anaerobic energy metabolism of Bacillus subtilis by arfM (ywiD). J. Bacteriol. 183 6815– 6821. 10.1128/JB.183.23.6815-6821.2001 11698370 PMC95522 · DOI · Paper page
  28. Morabbi Heravi K. Altenbuchner J. (2018). Cross talk among transporters of the phosphoenolpyruvate-dependent phosphotransferase system in Bacillus subtilis. J. Bacteriol. 200 e213– e218. 10.1128/JB.00213-18 30038046 PMC6148471 · DOI
  29. Müller T. Walter B. Wirtz A. Burkovski A. (2006). Ammonium toxicity in bacteria. Curr. Microbiol. 52 400– 406. 10.1007/s00284-005-0370-x 16604417 · DOI
  30. Nakano M. M. Hoffmann T. Zhu Y. Jahn D. (1998a). Nitrogen and oxygen regulation of Bacillus subtilis nasDEF Encoding NADH-dependent nitrite reductase by TnrA and ResDE. J. Bacteriol. 180 5344– 5350. 10.1128/JB.180.20.5344-5350.1998 9765565 PMC107582 · DOI
  31. Nakano M. M. Zuber P. Sonenshein A. L. (1998b). Anaerobic regulation of Bacillus subtilis krebs cycle genes. J. Bacteriol. 180 3304– 3311. 10.1128/JB.180.13.3304-3311.1998 9642180 PMC107282 · DOI
  32. Ongena M. Jacques P. (2008). Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16 115– 125. 10.1016/j.tim.2007.12.009 18289856 · DOI
  33. Pinhal S. Ropers D. Geiselmann J. de Jong H. (2019). Acetate metabolism and the inhibition of bacterial growth by acetate. J. Bacteriol. 201: e00147– 19. 10.1128/JB.00147-19 30988035 PMC6560135 · DOI
  34. Presecan-Siedel E. Galinier A. Longin R. Deutscher J. Danchin A. Glaser P. (1999). Catabolite regulation of the pta gene as part of carbon flow pathways in Bacillus subtilis. J. Bacteriol. 181 6889– 6897. 10.1128/JB.181.22.6889-6897.1999 10559153 PMC94162 · DOI
  35. Rangarajan V. Clarke K. G. (2015). Process development and intensification for enhanced production of Bacillus lipopeptides. Biotechnol. Genet. Eng. Rev. 31 46– 68. 10.1080/02648725.2016.1166335 27136722 · DOI
  36. Reents H. Munch R. Dammeyer T. Jahn D. Hartig E. (2006). The Fnr regulon of Bacillus subtilis. J. Bacteriol. 188 1103– 1112. 10.1128/JB.188.3.1103-1112.2006 16428414 PMC1347333 · DOI
  37. St-Pierre Lemieux G. Groleau D. Proulx P. (2019). Introduction on foam and its impact in bioreactors. Can. J. Biotechnol. 3 143– 157. 10.24870/cjb.2019-000131 · DOI
  38. Strohm T. O. Griffin B. Zumft W. G. Schink B. (2007). Growth yields in bacterial denitrification and nitrate ammonification. Appl. Environ. Microbiol. 73 1420– 1424. 10.1128/AEM.02508-06 17209072 PMC1828769 · DOI
  39. Willenbacher J. Rau J.-T. Rogalla J. Syldatk C. Hausmann R. (2015a). Foam-free production of surfactin via anaerobic fermentation of Bacillus subtilis DSM 10T. AMB Express 5: 21. 10.1186/s13568-015-0107-6 25852998 PMC4385232 · DOI
  40. Willenbacher J. Zwick M. Mohr T. Schmid F. Syldatk C. Hausmann R. (2014). Evaluation of different Bacillus strains in respect of their ability to produce Surfactin in a model fermentation process with integrated foam fractionation. Appl. Microbiol. Biotechnol. 98 9623– 9632. 10.1007/s00253-014-6010-2 25158834 · DOI
  41. Yanisch-Perron C. Vieira J. Messing J. (1985). Improved Ml3 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33 103– 119. 2985470

Cited by

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Authors
Hoffmann, M., Fernandez Cano Luna, D. S., Xiao, S., Stegemüller, L., Rief, K., Heravi, K. M., Lilge, L., Henkel, M., & Hausmann, R.
Affiliations
University of Hohenheim (DE)
Corresponding author
Henkel, Marius
Venue
Frontiers in Bioengineering and Biotechnology
Published
2020-11-26
Volume
8
Pages
554903-554903
ISSN
2296-4185 (ISSN-L)
OpenAlex
W3109513761
Cited by
37
References
2
Citations by year
2026: 7 · 2025: 4 · 2024: 7 · 2023: 4 · 2022: 8 · 2021: 7
FWCI
1.17
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Bioengineering and Biotechnology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Deutsche Forschungsgemeinschaft (365166982)
Topics
  • Physical Sciences › Environmental Science › Pollution › Microbial bioremediation and biosurfactants
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Physical Sciences › Chemistry › Organic Chemistry › Surfactants and Colloidal Systems
Keywords
surfactin, Bacillus subtilis, anaerobic cultivation, ammonium inhibition, nitrite, nitrate reductase, acetate accumulation, glucose concentration, specific growth rate, product yield, fed-batch fermentation, foaming, strain engineering, bioreactor scale-up

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