Skip to main content
Log in

Isolation and thermo-acclimation of thermophilic bacteria in hyperthermophilic fermentation system

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

Hyperthermophilic microorganisms play a key role in the hyper-thermophilic composting (HTC) technique. However, little information is available about the hyperthermophilic microorganisms prevalent in HTC systems, except for the Calditerricola satsumensis, Calditerricola yamamurae, and Thermaerobacter. To obtain effective hyper-thermophilic microorganisms, a continuous thermo-acclimation of the suitable thermophilic microorganisms was demonstrated in this study. Bacillus thermoamylovorans with high-temperature endurance (70 °C) were newly isolated from sludge composting, and an adequate slow heating rate (2 °C per cycle) was applied to further improve its thermostability. Finally, a strain with a maximum growth temperature of 80 °C was obtained. Moreover, structural and hydrophobic changes in cell proteins, the special amino acid content ratio, and the membrane permeability of the thermophilic bacterium after thermo-acclimation were evaluated for improved thermostability. In addition, the acclimated hyperthermophilic bacterium was further inoculated into the HTC system, and an excellent performance with a maximum operating temperature of 82 °C was observed.

Graphic abstract

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
Scheme 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  1. Zhou W, Liu M, Chai Y, Chen Y, Chen M, Wei Y, Min Y (2018) Discussion on establishment of technical standard system of domestic wastewater in villages and towns of China. Water Wastewater Eng 44(9):2–14. https://doi.org/10.13789/j.cnki.wwe1964.2018.0029

    Article  Google Scholar 

  2. Zhou G, Gu Y, Yuan H, Gong Y, Wu Y (2020) Selecting sustainable technologies for disposal of municipal sewage sludge using a multi-criterion decision-making method: a case study from China. Resour Conserv Recy 161:104881. https://doi.org/10.1016/j.resconrec.2020.104881

    Article  Google Scholar 

  3. Alves D, Villar I, Mato S (2019) Thermophilic composting of hydrocarbon residue with sewage sludge and fish sludge as cosubstrates: microbial changes and TPH reduction. J Environ Manag 239:30–37. https://doi.org/10.1016/j.jenvman.2019.03.028

    Article  CAS  Google Scholar 

  4. Song U, Lee EJ (2010) Environmental and economical assessment of sewage sludge compost application on soil and plants in a landfill. Resour Conserv Recy 54(12):1109–1116. https://doi.org/10.1016/j.resconrec.2010.03.005

    Article  Google Scholar 

  5. Tan XB, Yang LB, Zhang WW, Zhao XC (2020) Lipids production and nutrients recycling by microalgae mixotrophic culture in anaerobic digestate of sludge using wasted organics as carbon source. Bioresour Technol 297:122379. https://doi.org/10.1016/j.biortech.2019.122379

    Article  CAS  PubMed  Google Scholar 

  6. Raheem A, Sikarwar VS, He J, Dastyar W, Dionysiou DD, Wang W, Zhao M (2018) Opportunities and challenges in sustainable treatment and resource reuse of sewage sludge: a review. Chem Eng J 337:616–641. https://doi.org/10.1016/j.cej.2017.12.149

    Article  CAS  Google Scholar 

  7. Wu LJ, Higashimori A, Qin Y, Hojo T, Kubota K, Li YY (2016) Comparison of hyper-thermophilic–mesophilic two-stage with single-stage mesophilic anaerobic digestion of waste activated sludge: process performance and microbial community analysis. Chem Eng J 290:290–301. https://doi.org/10.1016/j.cej.2016.01.067

    Article  CAS  Google Scholar 

  8. Shao L, Wang T, Li T, Lü F, He P (2013) Comparison of sludge digestion under aerobic and anaerobic conditions with a focus on the degradation of proteins at mesophilic temperature. Bioresour Technol 140:131–137. https://doi.org/10.1016/j.biortech.2013.04.081

    Article  CAS  PubMed  Google Scholar 

  9. Zhang J, Chen G, Sun H, Zhou S, Zou G (2016) Straw biochar hastens organic matter degradation and produces nutrient-rich compost. Bioresour Technol 200:876–883. https://doi.org/10.1016/j.biortech.2015.11.016

    Article  CAS  PubMed  Google Scholar 

  10. Wei Y, Li J, Shi D, Liu G, Zhao Y, Shimaoka T (2017) Environmental challenges impeding the composting of biodegradable municipal solid waste: a critical review. Resour Conserv Recy 122:51–65. https://doi.org/10.1016/j.resconrec.2017.01.024

    Article  Google Scholar 

  11. Ge J, Huang G, Huang J, Zeng J, Han L (2015) Modeling of oxygen uptake rate evolution in pig manure-wheat straw aerobic composting process. Chem Eng J 276:29–36. https://doi.org/10.1016/j.cej.2015.04.067

    Article  CAS  Google Scholar 

  12. Onwosi CO, Igbokwe VC, Odimba JN, Eke IE, Nwankwoala MO, Iroh IN, Ezeogu LI (2017) Composting technology in waste stabilization: on the methods, challenges and future prospects. J Environ Manag 190:140–157. https://doi.org/10.1016/j.jenvman.2016.12.051

    Article  CAS  Google Scholar 

  13. Bialobrzewski I, Miks-Krajnik M, Dach J, Markowski M, Czekala W, Gluchowska K (2015) Model of the sewage sludge-straw composting process integrating different heat generation capacities of mesophilic and thermophilic microorganisms. Waste Manag 43(5):72–83. https://doi.org/10.1016/j.wasman.2015.05.036

    Article  CAS  PubMed  Google Scholar 

  14. Deive FJ, Domínguez A, Barrio T, Moscoso F, Morán P, Longo MA, Sanromán MA (2010) Decolorization of dye reactive black 5 by newly isolated thermophilic microorganisms from geothermal sites in Galicia (Spain). J Hazard Mater 182(1–3):735–742. https://doi.org/10.1016/j.jhazmat.2010.06.096

    Article  CAS  PubMed  Google Scholar 

  15. Sunil K (2011) Composting of municipal solid waste. Crit Rev Biotechnol 31(2):112–136. https://doi.org/10.3109/07388551.2010.492207

    Article  CAS  Google Scholar 

  16. Muibat OF, Ngole-Jeme VM, Babalola OO (2015) Diversity of acidophilic bacteria and archaea and their roles in bioremediation of acid mine drainage. Br Microbiol Res J 8(3):443–456. https://doi.org/10.9734/bmrj/2015/14365

    Article  Google Scholar 

  17. Bhattacharya A, Pletschke BI (2014) Thermophilic bacilli and their enzymes in composting. In: Dinesh KM (ed) Composting for sustainable agriculture, 6th edn. Springer, New York, pp 103–124

    Google Scholar 

  18. Yu Z, Tang J, Liao H, Liu X, Zhou P, Zhi C, Christopher R, Zhou S (2018) The distinctive microbial community improves composting efficiency in a full-scale hyperthermophilic composting plant. Bioresour Technol 265:146–154. https://doi.org/10.1016/j.biortech.2018.06.011

    Article  CAS  PubMed  Google Scholar 

  19. Liang J, Tang S, Gong J, Zeng G, Luo Y (2019) Responses of enzymatic activity and microbial communities to biochar/compost amendment in sulfamethoxazole polluted wetland soil. J Hazard Mater 385:121533. https://doi.org/10.1016/j.jhazmat.2019.121533

    Article  CAS  PubMed  Google Scholar 

  20. Bari Q, Koenig A, Guihe T (2010) Kinetic analysis of forced aeration composting- I. Reaction rates and temperature. Waste Manag Res 18(4):303–312. https://doi.org/10.1034/j.1399-3070.2000.00114.x

    Article  Google Scholar 

  21. Liu X, Hou Y, Li Z, Yu Z, Zhou S (2020) Hyperthermophilic composting of sewage sludge accelerates humic acid formation: elemental and spectroscopic evidence. Waste Manag 103:342–351. https://doi.org/10.1016/j.wasman.2019.12.053

    Article  CAS  PubMed  Google Scholar 

  22. Cui P, Liao H, Bai Y, Li X, Zhou S (2019) Hyperthermophilic composting reduces nitrogen loss via inhibiting ammonifiers and enhancing nitrogenous humic substance formation. Sci Total Environ 692:98–106. https://doi.org/10.1016/j.scitotenv.2019.07.239

    Article  CAS  PubMed  Google Scholar 

  23. Liao H, Lu X, Rensing C, Friman VP, Geisen S, Chen Z, Yu Z, Wei Z, Zhou S, Zhu Y (2017) Hyperthermophilic composting accelerates the removal of antibiotic resistance genes and mobile genetic elements in sewage sludge. Environ Sci Technol 52(1):266–276. https://doi.org/10.1021/acs.est.7b04483

    Article  CAS  PubMed  Google Scholar 

  24. Oshima T, Moriya TA (2008) Preliminary analysis of microbial and biochemical properties of high-temperature compost. Ann N Y Acad Sci 1125(1):338–344. https://doi.org/10.1196/annals.1419.012

    Article  CAS  PubMed  Google Scholar 

  25. Cheng Y, Inamori R, Ruike K, Inamori Y, Zhang Z (2018) Optimum dosage of hyper-thermophilic aerobic compost (HTAC) produced from sewage sludge for rice yield. Int J Bio 10(3):27. https://doi.org/10.5539/ijbv10n3p27

    Article  CAS  Google Scholar 

  26. Moriya T, Hikota T, Yumoto I, Ito T, Terui Y, Yamagishi A, Oshima T (2011) Calditerricola satsumensis gen. nov., sp. Nov. and Calditerricola yamamurae sp. Nov., extreme thermophiles isolated from a high-temperature compost. Int J Syst Evol Micr 61(3):631–636. https://doi.org/10.1099/ijs.0.018416-0

    Article  CAS  Google Scholar 

  27. Wang Z, Wu D, Lin Y, Wang X (2021) Role of temperature in sludge composting and hyperthermophilic systems: a Review. Bioenerg Res. https://doi.org/10.1007/s12155-021-10281-5

    Article  Google Scholar 

  28. Shiotsuka K, Tanaka A, Sakai K (2010) Occurrence of extreme thermophiles, thermaerobacter spp., in sewage sludge. J Jpn Soc Extrem 9(2):67–71. https://doi.org/10.3118/jjse.9.67

    Article  Google Scholar 

  29. Stetter KO (2013) A brief history of the discovery of hyperthermophilic life. Biochem Soc Trans 41(1):416–420. https://doi.org/10.1042/BST20120284

    Article  CAS  PubMed  Google Scholar 

  30. Steven DH, Bo-Barker J, Jay M, Anja B, Ruth B, Barry AC, Heribert C, Gerald RD, Timothy F, Kai-Uwe H, Nils GH, Richard M, Arthur S, Guizhi W, Barbara B, Bert E, Kathryn F, Glen G, Scott DR, Henrik SC, Gregory S, Ivano WA, Gilles G, Christopher HH, Fumio I, Patrick M, Thomas N, Sachiko NR, John DCS, Andreas T, Juergen W, Christian NP, Acosta JLS (2004) Distributions of microbial activities in deep subseafloor sediments. Science 306:2216–2221. https://doi.org/10.1126/science.1101155

    Article  CAS  Google Scholar 

  31. Atomi H, Sato T, Kanai T (2011) Application of hyperthermophiles and their enzymes. Curr Opin Biotechnol 22(5):618–626. https://doi.org/10.1016/j.copbio.2011.06.010

    Article  CAS  PubMed  Google Scholar 

  32. Vieille C, Zeikus GJ (2001) Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability. Microbiol Mol Biol Rev 65(1):1–43. https://doi.org/10.1128/MMBR.65.1.1-43.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sakuraba H, Goda S, Ohshima T (2010) Unique sugar metabolism and novel enzymes of hyperthermophilic archaea. Chem Rec 3(5):281–287. https://doi.org/10.1002/tcr.10066

    Article  CAS  Google Scholar 

  34. Pittera J, Jouhet J, Breton S, Garczarek L, Partensky F, Maréchal É, Nguyen NA, Doré H, Ratin M, Pitt FD (2017) Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus. Environ Microbiol 20(2):612–631. https://doi.org/10.1111/1462-2920.13985

    Article  CAS  PubMed  Google Scholar 

  35. Guyot S, Pottier L, Hartmann A, Ragon M, Hauck TJ, Molin P, Ferret E, Gervais P (2014) Extremely rapid acclimation of Escherichia coli to high temperature over a few generations of a fed-batch culture during slow warming. Microbiol Open 3(1):52–63. https://doi.org/10.1002/mbo3.146

    Article  CAS  Google Scholar 

  36. Rudolph B, Gebendorfer KM, Buchner J, Winter J (2010) Evolution of Escherichia coli for growth at high temperatures. J Biol Chem 285(25):19029–19034. https://doi.org/10.1074/jbc.M110.103374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Khan S, Farooq U, Kurnikova M (2016) Exploring protein stability by comparative molecular dynamics simulation of homologous hyperthermophilic, mesophilic and psychrophilic proteins. J Chem Inf Model 56:2129–2139. https://doi.org/10.1021/acs.jcim.6b00305

    Article  CAS  PubMed  Google Scholar 

  38. Sterpone F, Melchionna S (2012) Thermophilic proteins: insight and perspective from in silico experiments. Chem Soc Rev 41(5):1665–1676. https://doi.org/10.1039/c1cs15199a

    Article  CAS  PubMed  Google Scholar 

  39. Beadle BM, Baase WA, Wilson DB, Gilkes NR, Shoichet BK (1999) Comparing the thermodynamic stabilities of a related thermophilic and mesophilic enzyme. Biochemistry 38(8):2570–2576. https://doi.org/10.1021/bi9824902

    Article  CAS  PubMed  Google Scholar 

  40. Grimalt-Alemany A, Łężyk M, Kennes-Veiga D, Gavala SI, H, (2020) Enrichment of mesophilic and thermophilic mixed microbial consortia for syngas biomethanation: the role of kinetic and thermodynamic competition. Waste Biomass Valori 2:465–481. https://doi.org/10.1007/s12649-019-00595-z

    Article  CAS  Google Scholar 

  41. Gao X, Ding Y (2017) Using the residue interaction network improve the classification of thermophilic and mesophilic proteins. Curr Bioinform 12(3):249–257. https://doi.org/10.2174/1574893611666160502122132

    Article  CAS  Google Scholar 

  42. Brinda KV (2005) A network representation of protein structures: implications for protein stability. Biophys J 6(89):4159–4170. https://doi.org/10.1529/biophysj.105.064485

    Article  CAS  Google Scholar 

  43. Khadem H, Tirtouil A, Drabo S, Boubakeur B (2020) Ultrasound conditioning of Streptococcus thermophilus CNRZ 447: growth, biofilm formation, exopolysaccharide production, and cell membrane permeability. Biotechnologia 101:159–165. https://doi.org/10.5114/bta.2020.94774

    Article  CAS  Google Scholar 

  44. Qiu S, Ma F, Wo Y, Xu S (2010) Study on the biological effect of tourmaline on the cell membrane of E. coli. Surf Interface Anal 43:1069–1073. https://doi.org/10.1002/sia.3694

    Article  CAS  Google Scholar 

  45. Funnekotter B, Kaczmarczyk A, Turner SR, Bunn E, Zhou W, Smith S, Flematti G, Mancera RL (2013) Acclimation-induced changes in cell membrane composition and influence on cryotolerance of in vitro shoots of native plant species. Plant Cell Tiss Org 114(1):83–96. https://doi.org/10.1007/s11240-013-0308-0

    Article  CAS  Google Scholar 

  46. Xu L, Tian C, Lu X, Ling L, Lv J, Wu M, Zhu G (2015) Photoreactivation of Escherichia coli is impaired at high growth temperatures. J Photoch Photobio B 285(25):19029. https://doi.org/10.1016/j.jphotobiol.2015.03.012

    Article  CAS  Google Scholar 

  47. Ali ABA, Danial K, Asma A, Hoda B, Rosa F (2018) Identification of Thiobacillus bacteria in agricultural soil in Iran using the 16S rRNA gene. Mol Biol Rep 45(6):1723–1731. https://doi.org/10.1007/s11033-018-4316-3

    Article  CAS  Google Scholar 

  48. Geng WW, Yang G, Xie XY, Yang B (2009) Determination of protein hydrophobicity by sodium dodecyl sulfate binding method. Food Sci 30(24):416–418. https://doi.org/10.1007/978-3-540-85168-4_52

    Article  CAS  Google Scholar 

  49. Haralambiev L, Nitsch A, Jacoby M, Strakeljahn S, Stope B (2020) Cold atmospheric plasma treatment of chondrosarcoma cells affects proliferation and cell membrane permeability. Int J Mol Sci 21(7):2291. https://doi.org/10.3390/ijms21072291

    Article  CAS  PubMed Central  Google Scholar 

  50. Xiao Y, Zeng GM, Yang ZH, Shi WJ, Huang C, Fan CZ, Xu ZY (2009) Continuous thermophilic composting (CTC) for rapid biodegradation and maturation of organic municipal solid waste. Bioresour Technol 100(20):4807–4813. https://doi.org/10.1016/j.biortech.2009.05.013

    Article  CAS  PubMed  Google Scholar 

  51. Kulikowska D, Klimiuk E (2011) Organic matter transformations and kinetics during sewage sludge composting in a two-stage system. Bioresour Technol 102(23):10951–10958. https://doi.org/10.1016/j.biortech.2011.09.009

    Article  CAS  PubMed  Google Scholar 

  52. Gromiha MM, Pathak MC, Saraboji K, Ortlund EA, Gaucher EA (2013) Hydrophobic environment is a key factor for the stability of thermophilic proteins. Proteins 81(4):715–721. https://doi.org/10.1002/prot.24232

    Article  CAS  PubMed  Google Scholar 

  53. Pica A, Graziano G (2016) Shedding light on the extra thermal stability of thermophilic proteins. Biopolymers 105(12):856–863. https://doi.org/10.1002/bip.22923

    Article  CAS  PubMed  Google Scholar 

  54. Yuan H, Xu J, Van-Dam EP, Giubertoni G, Rezus YLA, Hammink R, Bakker HJ, Zhan Y, Rowan AE, Xing C (2017) Strategies to increase the thermal stability of truly biomimetic hydrogels: combining hydrophobicity and directed hydrogen bonding. Macromolecules 50(22):9058–9065. https://doi.org/10.1021/acs.macromol.7b01832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Hazel JR, Schuster VL (2010) The effects of temperature and thermal acclimation upon the osmotic properties and nonelectrolyte permeability of liver and gill mitochondria from rainbow trout (salmo gairdneri). J Exp Zool 195(3):425–438. https://doi.org/10.1002/jez.1401950309

    Article  Google Scholar 

  56. Blicher A, Wodzinska K, Fidorra M, Winterhalter M, Heimburg T (2008) The temperature dependence of lipid membrane permeability, its quantized nature, and the influence of anesthetics. Biophys J 96(11):4581–4591. https://doi.org/10.1016/j.bpj.2009.01.062

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge that this work was supported by the National Natural Science Foundation of China (22078194) and National Key Research and Development Program (2017YFE0127100).

Funding

Funding provided by the National Natural Science Foundation of China (22078194) and National Key Research and Development Program (2017YFE0127100).

Author information

Authors and Affiliations

Authors

Contributions

ZW: conceptualization, investigation, methodology, experiments and writing (original draft preparation). SW: article revision and supervision. CF: methodology and article revision. XZ: data collection and writing (review and editing). DW: methodology and investigation. XW: formal analysis and investigation. HK: methodology, writing (review and editing), supervision and funding acquisition.

Corresponding authors

Correspondence to Xiangyong Zheng or Hainan Kong.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Wu, S., Fan, C. et al. Isolation and thermo-acclimation of thermophilic bacteria in hyperthermophilic fermentation system. Bioprocess Biosyst Eng 45, 75–85 (2022). https://doi.org/10.1007/s00449-021-02640-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-021-02640-5

Keywords

Navigation