Journal of Polymers and the Environment

, Volume 27, Issue 12, pp 2793–2803 | Cite as

Biodegradation of Cellulose in Laboratory-Scale Bioreactors: Experimental and Numerical Studies

  • Antonis MistriotisEmail author
  • Nikoleta-Georgia Papardaki
  • Astero Provata
Original paper


Standard tests such as ISO 17556 (Plastics - determination of the ultimate aerobic biodegradability in soil by measuring the oxygen demand in a respirometer or the amount of carbon dioxide evolved. International Organization for Standardization, Geneva, Switzerland, 2019) or ASTM D5988 (Standard test method for determining aerobic biodegradation of plastic materials in soil. ASTM International, West Conshohocken, 2018) have been developed for measuring the biodegradation of polymers and assessing their biodegradability in soil. In several experiments performed according to these standard tests, the measured biodegradation of cellulose was reported unexpectedly between 80 and 85%. These results are difficult to justify since cellulose is a well-known biodegradable material. In the present study, this phenomenon is explained as the consequence of starvation occurring in a confined bioreactor. It is proposed that the favourable conditions applied to the small-size bioreactors accelerate the proliferation of the microorganisms which are responsible for the biodegradation. Such a dense microbial population may face starvation when cellulose is consumed. It is assumed that starvation causes the secretion of an inhibitory chemical signal, which can diffuse to neighbouring sites still containing food, and suppresses biodegradation. This hypothesis was supported by two experiments. First, it was shown that the final measured biodegradation increased when the microbial growth rate decreased by reducing temperature. In the second experiment, it was shown that the biodegradation proceeded slower when a new cellulose quantity was inserted into a previously used soil substrate. To confirm the hypothesis regarding the presence of an inhibitory starvation factor, which can suppress biodegradation, a Kinetic Monte Carlo (KMC) model was also developed. The KMC simulations reproduced qualitatively the experimental findings.


Biodegradation Cellulose Starvation of microorganisms Standard tests for biodegradation Small-scale bioreactors Kinetic Monte Carlo simulations 



The authors would like to thank Professor D. Briassoulis for his support and for many fruitful discussions. This work was supported by computational time granted from the Greek Research & Technology Network (GRNET) in the National HPC facility–ARIS, under Project ID: PR007011.

Supplementary material

10924_2019_1560_MOESM1_ESM.xlsx (23 kb)
Supplementary material 1 (XLSX 23 kb)


  1. 1.
    ISO 17556 (2019) Plastics - determination of the ultimate aerobic biodegradability in soil by measuring the oxygen demand in a respirometer or the amount of carbon dioxide evolved. International Organization for Standardization, GenevaGoogle Scholar
  2. 2.
    ASTM D 5988-12 (2018) Standard test method for determining aerobic biodegradation of plastic materials in soil. ASTM International, West ConshohockenGoogle Scholar
  3. 3.
    Plastics Europe, Plastics – the Facts 2017 (2017) An analysis of European plastics production, demand and waste data. Plastics Europe, Association of plastics manufacturers.
  4. 4.
    Hopewell J, Dvorak R, Kosior E (2009) Plastic recycling: challenges and opportunities. Philos Trans R Soc B364:2115–2126CrossRefGoogle Scholar
  5. 5.
    UN Environment (2017) Clean seas, turn the tide on plastic. United Nations Environment Programme.
  6. 6.
    Briassoulis D, Degli Innocenti F (2017) Chapter 6: standards for soil biodegradable plastics. In: Malinconico M (ed) Soil degradable bioplastics for a sustainable modern agriculture. Green chemistry and sustainable technology. Springer, Berlin, pp 139–168CrossRefGoogle Scholar
  7. 7.
    ISO 14855–1 (2012) Determination of the ultimate aerobic biodegradability of plastic materials under controlled composting conditions – Method by analysis of evolved carbon dioxide – Part 1: General method. International Organization for Standardization, GenevaGoogle Scholar
  8. 8.
    Eichorst SA, Kuske CR (2012) Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl Environ Microbiol 78:2316–2327CrossRefGoogle Scholar
  9. 9.
    Briassoulis D, Mistriotis A (2018) Key parameters in testing biodegradation of bio-based materials in soil. Chemosphere 207:18–26CrossRefGoogle Scholar
  10. 10.
    López Alvarez JV, Aguilar Larrucea M, Arraiza Bermúdez P, León Chicote B (2009) Biodegradation of paper waste under controlled composting conditions. Waste Manage 29:1514–1519CrossRefGoogle Scholar
  11. 11.
    Bettas Ardisson G, Tosin M, Barbale M, Degli-Innocenti F (2014) Biodegradation of plastics in soil and effects on nitrification activity. A laboratory approach. Front Microbiol 5:710CrossRefGoogle Scholar
  12. 12.
    Puget P, Angers DA, Chenu C (1999) Nature of carbohydrates associated with water-stable aggregates of two cultivated soils. Soil Biol Biochem 31:55–63CrossRefGoogle Scholar
  13. 13.
    Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379PubMedPubMedCentralGoogle Scholar
  14. 14.
    Matin A (1991) The molecular basis of carbon-starvation-induced general resistance in Escherichia coli. Mol Microbiol 5:3–10CrossRefGoogle Scholar
  15. 15.
    Szilagyi M, Miskei M, Karanyi Z, Lenkey B, Pocsi I, Emri T (2013) Transcriptome changes initiated by carbon starvation in Aspergillus nidulans. Microbiology 159:176–190CrossRefGoogle Scholar
  16. 16.
    Xiong Y, Coradetti ST, Li X, Gritsenko MA, Clauss T, Petyuk V, Camp D, Smith R, Cate JHD, Yang F, Glass NL (2014) The proteome and phosphoproteome of Neurospora crassa in response to cellulose, sucrose and carbon starvation. Fungal Genet Biol 72:21–33CrossRefGoogle Scholar
  17. 17.
    Lodish H., Berk A., Kaiser C.A., Krieger M., Bretscher A., Ploegh H., Amon A., Scott M.P., (2013), Molecular Cell Biology. W. H. Freeman and Co., 7th edition – Chapter 15Google Scholar
  18. 18.
    Newell PC (1978) Cellular communication during aggregation of Dictyostelium. J Gen Microbiol 104:1–13CrossRefGoogle Scholar
  19. 19.
    Clarke M, Gomer RH (1995) PSF and CMF, autocrine factors that regulate gene expression during growth and early development of Dictyostelium. Experientia 51:1124–1134CrossRefGoogle Scholar
  20. 20.
    Stephan J, Vattuone L, Rogowska JM, Burghaus U (2006) A practical guide to kinetic monte carlo simulations and classical molecular dynamics simulations. Nova Science Pub Inc., HauppaugeGoogle Scholar
  21. 21.
    Jansen APJ (2012) An introduction to kinetic Monte Carlo simulations of surface reactions, 856. Lecture notes in Physics. Springer, BerlinCrossRefGoogle Scholar
  22. 22.
    Noussiou VK, Provata A (2007) Surface reconstruction in reactive dynamics: a kinetic Monte Carlo approach. Surf Sci 601:2941–2951CrossRefGoogle Scholar
  23. 23.
    Shabunin A, Provata A (2013) Lattice limit cycle dynamics: influence of long-distance reactive and diffusive mixing. Eur Phys J 222:2547–2557Google Scholar
  24. 24.
    Den Biggelaar C (2004) Soil sampling. agroecology lab manual and readings, Appalachian State University.
  25. 25.
    Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38CrossRefGoogle Scholar
  26. 26.
    Bremner DC, Mulvaney JM (1982) Total nitrogen. In: Page AL, Miller RH, Keaney DR (eds) Methods of soil analysis, Number 9 Part 2. American Society of Agronomy, MadisonGoogle Scholar
  27. 27.
    ISO 10390 (2005) Soil quality – Determination of pH. International Organization for Standardization, GenevaGoogle Scholar
  28. 28.
    Lamas F, Irigaray C, Oteo C, Chacon J (2005) Selection of the most appropriate method to determine the carbonate content for engineering purposes with particular regard to marls. Eng Geol 81(2005):32–41CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Natural Resources and Agricultural EngineeringAgricultural University of AthensAthensGreece
  2. 2.Institute of Nanoscience and NanotechnologyNational Center for Scientific Research “Demokritos”AthensGreece

Personalised recommendations