Determination of growth kinetics of microorganisms linked with 1,4-dioxane degradation in a consortium based on two improved methods

Abstract

● Evaluated three methods for determining the consortia’s growth kinetics.

● Conventional method is flawed since it relies on the total biomass concentration.

● Considering only selected bacterial taxa improved the accuracy.

● Considering oligotrophs and copiotrophs further improved the accuracy.

The conventional method for determining growth kinetics of microbial consortia relies on the total biomass concentration. This may be inaccurate for substrates that are uncommon in nature and can only be degraded by a small portion of the microbial community. 1,4-dioxane, an emerging contaminant, is an example of such substrates. In this work, we evaluated an improved method for determining the growth kinetics of a 1,4-dioxane-degrading microbial consortium. In the improved method, we considered only bacterial taxa whose concentration increase correlated to 1,4-dioxane concentration decrease in duplicate microcosm tests. Using PEST (Parameter Estimation), a model-independent parameter estimator, the kinetic constants were estimated by fitting the Monod kinetics-based simulation results to the experimental data that consisted of the concentrations of 1,4-dioxane and the considered bacterial taxa. The estimated kinetic constants were evaluated by comparing the simulation results with experimental results from another set of microcosm tests. The evaluation was quantified by the sum of squared relative residual, which was four orders of magnitude lower for the improved method than the conventional method. By further dividing the considered bacterial taxa into oligotrophs and copiotrophs, the sum of squared relative residual further decreased.

Graphical abstract

Keywords

Biodegradation / 1,4-Dioxane / Kinetics / Microbial consortium / 16S rRNA

References

[1] AdamsonD T WilsonJ T FreedmanD L Ramos-GarcíaA A LebrónC DankoA( 2022). Establishing the prevalence and relative rates of 1,4-dioxane biodegradation in groundwater to improve remedy evaluations. Journal of Hazardous Materials, 424(Pt D): 127736

[2] AoyagiT, MorishitaF, SugiyamaY, IchikawaD, MayumiD, KikuchiY, OgataA, MuraokaK, HabeH, HoriT. (2018). Identification of active and taxonomically diverse 1,4-dioxane degraders in a full-scale activated sludge system by high-sensitivity stable isotope probing. The ISME Journal, 12( 10): 2376– 2388

[3] Barajas-RodriguezF J, FreedmanD L. (2018). Aerobic biodegradation kinetics for 1,4-dioxane under metabolic and cometabolic conditions. Journal of Hazardous Materials, 350 : 180– 188

[4] ChenD Z, JinX J, ChenJ, YeJ X, JiangN X, ChenJ M. (2016). Intermediates and substrate interaction of 1,4-dioxane degradation by the effective metabolizer Xanthobacter flavus DT8. International Biodeterioration & Biodegradation, 106 : 133– 140

[5] ChenR, MiaoY, LiuY, ZhangL, ZhongM, AdamsJ M, DongY, MahendraS. (2021). Identification of novel 1,4-dioxane degraders and related genes from activated sludge by taxonomic and functional gene sequence analysis. Journal of Hazardous Materials, 412 : 125157

[6] ChungJ LeeG Chung S LeeY W ( 2019). Removal of 1,4-Dioxane in Water Using Specific Microbe Immobilization Cells. Water, Air, & Soil Pollution, 230(6): 114

[7] DohertyJ MuffelsC RumbaughJ TonkinM ( 2014). PEST, Model independent parameter estimation and uncertainty analysis

[8] EnvironmentalProtection Agency (USEPA) ( 2017). Technical Fact Sheet – 1,4-Dioxane;

[9] GradyP L, SockS M, CowanR M. (1997). A Critical component in the scale-up of wastewater treatment systems. Biotechnology in the Sustainable Environment, 54 : 307– 308

[10] HeY, MathieuJ, YangY, YuP, da SilvaM L B, AlvarezP J J. (2017). 1,4-dioxane biodegradation by Mycobacterium dioxanotrophicus PH-06 is associated with a group-6 soluble di-iron Monooxygenase. Environmental Science & Technology Letters, 4( 11): 494– 499

[11] InoueD, TsunodaT, SawadaK, YamamotoN, SaitoY, SeiK, IkeM. (2016). 1,4-dioxane degradation potential of members of the genera Pseudonocardia and Rhodococcus. Biodegradation, 27( 4−6): 277– 286

[12] InoueD, TsunodaT, YamamotoN, IkeM, SeiK. (2018). 1,4-Dioxane degradation characteristics of Rhodococcus aetherivorans JCM 14343. Biodegradation, 29( 3): 301– 310

[13] IonescuD OverholtW A LynchM D NeufeldJ D NaqibA GreenS J ( 2016). Microbial community analysis using high-throughput amplicon sequencing. In: Manual of Environmental Microbiology, 4th ed, 2–4

[14] JinX, ChenD, ZhuR, ChenJ, ChenJ. (2012). Characteristics of 1,4-dioxane degradation by Xanthobacter flavus DT8. Environmental Sciences, 33( 5): 1657– 1662

[15] KämpferP KroppenstedtR M( 2004). Pseudonocardia benzenivorans sp . nov. International Journal of Systematic and Evolutionary Microbiology, 54(Pt 3): 749–751

[16] KochA L. (2001). Oligotrophs versus copiotrophs. BioEssays, 23( 7): 657– 661

[17] KruskalJ B. (1964). Nonmetric multidimensional scaling: a numerical method. Psychometrika, 29( 2): 115– 129

[18] MaF, WangY, YangJ, GuoH, SuD, YuL. (2021). Degradation of 1,4-dioxane by Xanthobacter sp. YN2. Current Microbiology, 78( 3): 992– 1005

[19] MahendraS, Alvarez-CohenL. (2006). Kinetics of 1,4-dioxane biodegradation by monooxygenase-expressing bacteria. Environmental Science & Technology, 40( 17): 5435– 5442

[20] MohrT K StickneyJ A DiGuiseppiW H ( 2010). Environmental Investigation and Remediation: 1,4-Dioxane and Other Solvent Stabilizers. Boca Raton: CRC Press

[21] NamJ H, VenturaJ S, YeomI T, LeeY, JahngD. (2016). Structural and Kinetic characteristics of 1,4-dioxane-degrading bacterial consortia containing the phylum TM7. Journal of Microbiology and Biotechnology, 26( 11): 1951– 1964

[22] OksanenJ, KindtR, LegendreP, O’HaraB, StevensM H H, OksanenM J, SuggestsM. (2007). The vegan package. Community Ecology Package, 10 : 631– 637

[23] PropsR, KerckhofF M, RubbensP, De VriezeJ, Hernandez SanabriaE, WaegemanW, MonsieursP, HammesF, BoonN. (2017). Absolute quantification of microbial taxon abundances. The ISME Journal, 11( 2): 584– 587

[24] PugazhendiA, BanuJ R, DhavamaniJ, YeomI T. (2015). Biodegradation of 1,4-dioxane by Rhodanobacter AYS5 and the role of additional substrates. Annals of Microbiology, 65( 4): 2201– 2208

[25] PylroV S, RoeschL F W, MoraisD K, ClarkI M, HirschP R, TótolaM R. (2014). Data analysis for 16S microbial profiling from different benchtop sequencing platforms. Journal of Microbiological Methods, 107 : 30– 37

[26] RasM, Girbal-NeuhauserE, PaulE, SpérandioM, LefebvreD. (2008). Protein extraction from activated sludge: an analytical approach. Water Research, 42( 8−9): 1867– 1878

[27] RoyD Anagnostu G ChaphalkarP ( 1994). Biodegradation of dioxane and diglyme in industrial waste. Journal of Environmental Science and Health, Part A, Environmental Science and Engineering and Toxicology, 29(1): 129− 147

[28] SeiK, MiyagakiK, KakinokiT, FukugasakoK, InoueD, IkeM. (2013). Isolation and characterization of bacterial strains that have high ability to degrade 1,4-dioxane as a sole carbon and energy source. Biodegradation, 24( 5): 665– 674

[29] SockS M A ( 1993). Comprehensive evaluation of biodegradation as a treatment alternative for the removal of 1,4-dioxane. Dissertation for the Master’s Degree. Clemson: Clemson University U.S

[30] XiongY, MasonO U, LoweA, ZhouC, ChenG, TangY. (2019). Microbial community analysis provides insights into the effects of tetrahydrofuran on 1,4-dioxane biodegradation. Applied and Environmental Microbiology, 85( 11): e00244– e19

[31] YamamotoN SaitoY InoueD SeiK Ike M ( 2018). Characterization of newly isolated Pseudonocardia sp . N23 with high 1,4-dioxane-degrading ability. Journal of Bioscience and Bioengineering, 125(5): 552–558

[32] ZenkerM J, BordenR C, BarlazM A. (2002). Modeling cometabolism of cyclic ethers. Environmental Engineering Science, 19( 4): 215– 228

[33] ZhouC XiongY TangY DworatzekS (2018). 1,4-Dioxane Biodegradation at Low Concentrations. 2018. Battelle Chlorinated Conference

[34] ZhouY, HuangH, ShenD. (2016). Multi-substrate biodegradation interaction of 1,4-dioxane and BTEX mixtures by Acinetobacter baumannii DD1. Biodegradation, 27( 1): 37– 46

RIGHTS & PERMISSIONS

Higher Education Press