Hydrogen utilization rate: A crucial indicator for anaerobic digestion process evaluation and monitoring

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    benecial for maintaining H2 partial pressure in an appropriately low level. Moreover, such system was thermody-

    Anaerobtechnologycess, at leasacetogenic borganic comin which i

    appropriate for evaluating anaerobic degradability of contaminantsfully is essential.

    In AD process, methanogenic archaea, which catalyze the ter-minal stage of the process, are generally divided into two maingroups, i.e., acetoclastic methanogenes (convert acetate into CH4)and hydrogenotrophic methanogenes (convert H2/CO2 into CH4),

    stic meth-ately 70%

    hanogeneslow partialtermediateported that

    of different microbial groups in AD process; however, few studieshave focused on determining the activity of hydrogenotrophicmethanogens (13,17). Gijzen et al. (18) proposed a hydro-genotrophic methanogenic activity test that uses formic acid assubstrate. However, the consumption rate of formic acid is unableto reect H2 utilisation potential of hydrogenotrophicmethanogensdirectly. In addition, the test procedure was not elucidated andfactors that inuence the hydrogen utilization rate (HUR) test werenot discussed. Leu et al. (19) developed a kinetic model based on

    * Corresponding author. Tel.: 86 13402987449; fax: 86 029 82201354.

    Journal of Bioscience aVOL. 117 No. 4, 51digester performance (8). However, studies on full-scale anaerobicsystems have found that H2 determination, combined with ther-modynamic calculations, is not sufcient for providing meaningfulinformation on actual AD systems (9,10). The metabolic potentialsof anaerobic sludge cannot be assumed to be the same, even if theH2 partial pressure of different anaerobic systems is maintained onan equivalent level. Therefore, determining other parameters

    few studies have focused on the development of efcient anaerobicprocesses by enriching hydrogenotrophic methanogens (15,16).Therefore, determining the activity of hydrogenotrophic metha-nogens, which can be used to indicate the regulating capacity of H2partial pressure by this type of methanogens in reactors, is veryessential.

    Numerous criteria can be used for evaluatingmicrobial activitiesoxidized to acetate, is a key step in organic methanogenic conver-sion. In order to keep acetogenesis process thermodynamicallyfeasible, low H2 partial pressure (

  • the test vials (13,21). Therefore, a simple and more reliable testapproach for hydrogenotrophic methanogenic activity should be

    HUR dcH2dt

    V 1X

    (1)

    HUR 0:633 24 HUR 0:633 24 dcH2dt

    VX

    (2)

    where dcH2 =dt is the H2 consumption rate in the reactor (h1), V is the headspace

    volume (mL), X is the total biomass in the reactor (gVSS) and 0.633 is the conversioncoefcient of hydrogen to oxygen at 35C.

    c systems in the study period evaluated in the survey.

    Flow rate(m3/d)

    Reactorvolume(m3)

    MLVSS(g/L)

    CODinf(mg/L)

    CODeff(mg/L)

    HRT(h)

    Nv (gCOD/(L$ d))

    SRT(d)

    0.0045 0.0045 12.92 4000 110 24 4.0 20.0

    750 1300 20.0 8000 1000 e 1200 41.5 4.62 27.0

    2000 820 17.30 1800 500 e 700 10 e 12 4.39 36.01400 300 13.07 1000 300 15 3.33 /400 240 15.97 1200 350 10 e 15 5.0 /

    J. BIOSCI. BIOENG.,developed.In the present study, a volumetric test device and a test proce-

    dure were developed for measuring HUR of anaerobic sludge. Theinuences of HUR on specic methanogenic activity (SMA) andreactor performance were also discussed.

    MATERIALS AND METHODS

    Sludge samples Sludge samples were respectively from ve differentanaerobic reactors. A summary of the compiled average operational data for thestudy period is shown in Table 1. To enable the residual matrix to achieve completeconsumption, portions of all sludge samples were elutriated with oxygen-free waterand reacclimatized for 8 he12 h at 35C prior to HUR and SMA determination.

    The experimental HUR test device A new volumetric experimental device,shown in Fig. 1, was designed for monitoring HUR of anaerobic systems. The reactorwas made of glass and had a volume of 1.0 L. A higher height-to-diameter ratio (H/D:3) was selected to maintain highly efcient H2 transmission. Liquid agitation wasachieved by employing a magnetic stirrer and an H2 supplement that uses a gaslift system by recirculating headspace gas through a peristaltic pump. To makepressure within the reactor in equilibrium to atmospheric pressure, amicromanometer was used to monitor gas pressure in the vial headspace andprediction agrees well with the experimental value, determinationand optimization of parameters, as well as the subsequent modelsolution and validation are relatively difcult and time-consumingto conduct. Coates et al. (20) developed an assay method bydetecting manometric change of headspace pressure for measuringhydrogenotrophic methanogenic activity of anaerobic sludge.Although this manometric test is easy to conduct, it is not suf-ciently accurate for reecting actual activity of hydrogenotrophicmethanogens because balance between the dissolution and evac-uation of CO2 cannot be controlled. Bicarbonate in the inoculumsmay contribute to surplus of CO2 during the experiment. Moreover,the residual organics in inoculums will also produce excess CO2,thus resulting in changes in the liquidegas equilibrium of CO2 in

    TABLE 1. Average operational data of the anaerobi

    Treatmentprocess

    pH Workingtemperature

    (C)

    Lab-scale CSTR (with glucoseas the sole carbon source)

    CSTR 7.2 351

    Industrial wastewatertreatment facilitiesin Xian

    GuoWei starchfactory

    UASB1 7.0 351

    Hans brewery UASB2 7.1Wan Long paper mill UASB3 7.3Xian Coca-ColaBeverages Co.

    UASB4 7.1

    520 HOU ET AL.inert gas N2 served as the balance gas. The reactor sealing test was conductedbefore HUR testing.

    HUR test procedure Using the device shown in Fig. 1, the detailedexperimental procedures are as follows. Firstly, an appropriate sludge sample witha buffer solution was deposited into the reactor, and liquor pH was maintained atapproximately 7.0. The buffer solution contained 0.2 g NH4Cl, 0.08 g KH2PO4 and2.0 g NaHCO3 per litre of oxygen-free water. The reactor was sealed with gas-tightrubber septa. Secondly, an appropriate volume of pure H2 gas was introduced intothe reactor to replace the supernatant buffer solution. The peristaltic pump wasopened to cycle H2 gas continuously in the reactor. Meanwhile, the magneticstirrer was turned on to launch the test. To balance gas pressure in the reactorheadspace with atmospheric pressure, a U gauge was used to monitor pressurewithin the reactor and inert gas N2 served as a balance gas. Since the test wasinitiated, headspace gas was sampled regularly (once per 0.5 h) and analyzed bygas chromatography (GC). At the end of the HUR test, the amount of biomasspresent in the reactors was quantied in terms of volatile suspended solids (VSS)by ashing the sludge pellet obtained via gravimetric method (22).

    HUR calculation The decrease in H2 concentration obtained by GC could beconverted into HUR with a unit of mL-H2/(gVSS$h) using Eq. 1 and a unit of gCOD/(gVSS$d) using Eq. 2, as follows:Gas analyses H2 and CH4 were measured using an Agilent gas chromato-graph (Agilent 6890N GC, Agilent Technologies, CA, USA), equipped with a TDX-01packed column (2 m 0.3 mm) and a thermal conductivity detector (TCD). Theinert gas argon was selected as the carrier gas at a ow rate of 49.9 mL/min. Thecolumn, injection port and detector temperatures were 100C, 120C and 160C,respectively. The headspace gas in the reactor was sampled using a 500 mL pressure-lock syringe (Unimetrics, CA, USA), followed by direct injection into the columnthrough a septum. The gas volume percentage (Ci) was got from the data-processingsoftware of the GC. H2 partial pressure was calculated according to the followingequation:

    pH2 101325 CH2 (3)

    SMA test To examine the specic maximum anaerobic uptake rate of diversesubstrates for generating CH4, the SMA test was conducted in 250 mL serum bottlesat 35 1C under anaerobic conditions.

    The sludge concentration of the serum bottle was approximately 5 gVSS/L. Ac-etate, propionate and butyrate were used as the substrate for anaerobic microbesgenerating CH4, and the initial concentration was prepared in 4000 mg/L. Prior toaddition into the test bottles, the substrate solution was adjusted to approximatelypH 7.0. CH4 productionwasmeasured at a regular time interval (once every 1 h) afterFIG. 1. Schematic diagram of the HUR test device: 1, serum bottle; 2, magnetic mixer;3, gas diffuser; 4, rotor; 5, sealing plug; 6, peristaltic pump; 7, balance gas bag (N2);8, valve; 9, micromanometer. The volumetric experimental device was designed formonitoring HUR of anaerobic system.

  • values of HUR were 34.52 22.0, 46.02 29.33, 69.03 44.0,92.17 58.67 and 138.06 88.0 mL-H2/(gVSS$h), respectively. Itcan be seen that the calculated values of HUR were greater than theexperimental values. Hence, the experimental results were reliableand the experimental procedure for the HUR test was technicallyfeasible.

    The test vials (600mL) containing 400mL sludge/buffer solutionand the residual headspace was lled with anaerobic H2 gas. All thetested vials followed the same speed of liquid agitation and biogasrecycling ratio. In summary, the experimental results demonstratedthat HUR value highly depended on the sludge concentrations inthe test vessel because of H2 mass transfer limitation. The HURvalue increased with decreasing sludge concentration over the testrange, and the maximum HUR was obtained when the sludgeconcentration decreased to 1.0 gVSS/L. Therefore, the critical sludgeconcentration in the test bottle was identied to 1 g/L. Themaximum HUR could be achieved only when the sludge concen-tration was equal to or less than 1.0 gVSS/L. The test results for thesludge concentrations of 0.5 gVSS/L and 0.75 gVSS/L furtherconrmed the efciency of the aforementioned optimal sludgeconcentration.

    05

    10152025

    0.0 0.5 1.0 1.5 2.0 2.5MLVSS (g/L)

    HUR

    ( m

    L-H2

    /(gV

    FIG. 2. Effects of sludge concentration on HUR value. To investigate the effect ofbiomass concentration on the HUR test, ve sludge concentrations, namely, 0.5, 0.75,1.0, 1.5 and 2.0 gVSS/L were sampled from the lab-scale CSTR reactor to conduct aseries of contrast tests (A), and the results showed that the threshold sludge con-centration was 1 g/L for the maximum HUR test (B).the test was initiated, and the precise biomass was quantied using the gravimetricmethod (22). Finally, SMA was calculated according to the following equation:

    mmax,CH4 1

    0:395 dVCH4

    dt 1XV

    (4)

    where mmax,CH4 is the maximum SMA [gCOD/(gVSS$ d)], 1/0.395 is the conversion

    coefcient of CH4 to oxygen at 35C,dVCH4dt is the CH4 production rate (L-CH4/d) and XV

    is the total biomass present in the serum bottle (gVSS).

    RESULTS AND DISCUSSION

    Optimization of assay condition H2 is a poorly soluble gas(Henrys constant of 7.4 104 mol/(L$ Pa) at 35C) (23) andpresents a relatively low mass transfer coefcient. Thus, the H2/CO2 utilization rate of hydrogenotrophic methanogens will belimited by the hydrogen available in the aqueous phase (17,24). Inorder to test the maximum activity of hydrogenotrophicmethanogens, H2 gas has to be transferred to the liquid phase atsuch a rate that its dissolved concentrations do not restrain thekinetics of methanogenesis (25). H2 mass transfer under a steadystate can be expressed by the following equation:

    dC=dt KLaC* C

    (5)

    where dC/dt is the mass transfer rate, KLa is the total mass transfercoefcient, C* is the saturation concentration of dissolved hydrogenand C is the concentration of dissolved hydrogen.

    KLa is the main factor for H2 gas mass transfer rate as indicatedin Eq. 5. Pauss et al. (23) stated that the value of KLa is partlyinuenced by the volumetric gas supply rate. KLa also depends onthe specic surface area between H2 gas and the liquor phase.

    To improve H2 mass transfer rate, a high H/D (3.0) of the reactorand the ne-bubble diffuser was selected. A higher H/D can prolonggas retention time in the liquor. Moreover, the ne-bubble diffusercan make H2 dispersed into water in very ne bubbles, therebyincreasing the area of the liquor/gas interface. Frigon and Guiot (5)indicated that the liquid/gas interface can be increased by biogasrecycling. Accordingly, this previous study employed a 2:1 gas-recycling ratio in the system to enhance mass transfer rate.

    The gaseliquid interface area and H2 mass transfer rate aresignicantly affected by sludge concentration. To investigate theeffect of biomass concentration on the HUR test referring to theviewpoint of elsewhere (20), ve sludge concentrations, namely,0.5, 0.75, 1.0, 1.5 and 2.0 gVSS/L were sampled from the lab-scaleCSTR reactor to conduct a series of contrast tests. Thereby, theoptimum sludge concentration was obtained.

    The decrease in H2 gas volume over time under different sludgeconcentrations is illustrated in Fig. 2A. Considerable H2 gas wasconsumed and high H2 gas reductions were observed with highersludge concentrations. Nevertheless, the HUR value that corre-sponds to high sludge concentration was not the maximum rate.The H2 mass transfer was restricted under high sludge concentra-tion, thereby resulting in an underestimation of the methanogenicactivity on H2. HUR remained unchanged until sludge concentra-tion was less than 1 g/L (Fig. 2B). The experiments were repeatedand the same results were obtained. Therefore, 1 g/L sludge con-centration was identied as the threshold of the maximum HURtest. This nding indicates that if the sludge concentration isgreater than the threshold point, H2 gas transfer will be limited andthe determined HUR value will be underestimated. H2 uptake bybiomass will not be restricted by H2 mass transfer limitation andthe maximum HUR can be reached only when the sludge concen-

    VOL. 117, 2014tration is less than the threshold point.The KLa value of 4.11 2.62 h1 proposed by Frigon and Guiot

    (5) was used to calculate the theoretical value of HUR.When sludgeconcentrations were 2.0, 1.5, 1.0, 0.75 and 0.5 g/L, the calculated160

    170

    180

    190

    200

    210

    0 0.5 1 1.5 2 2.5Time (h)

    H2vo

    lum

    e (mL

    )

    0.5 g/L0.75 g/L1.0 g/L1.5 g/L2.0 g/L

    303540

    SSh))

    A

    B

    SIGNIFICANCE OF HUR FOR EVALUATING AD PROCESS 521Relationship between H2 partial pressure andHUR Hydrogenotrophic methanogenic species play a key rolein overall AD process. These species maintain an insignicantly lowH2 partial pressure (

  • was observed as HUR test value increased from 0.97 gCOD/(gVSS$d) to 2.46 gCOD/(gVSS$ d) (Fig. 5). This phenomenon can beexplained by the hypothesis that an increase in HUR will reduceH2 concentration in the system, thereby improving intermediateVFAs degradation rates. An improvement in intermediatedegradation will allow AD process to avoid acid accumulation,

    0

    20

    40

    60

    80

    100

    CSTR UASB1 UASB2 UASB3 UASB4

    H2

    parti

    al p

    ress

    ure

    (Pa)

    0.0

    0.2

    0.4

    0.6

    0.8

    1.0

    SMA

    -pro

    pion

    ate

    (gCO

    D/(gV

    SSd

    )

    H2 partial pressure SMA-propionate

    A

    B

    100

    CSTR UASB1 UASB2 UASB3 UASB4

    0.8 ))

    H2 partial pressure SMA-butyrate

    FIG. 4. Relationships between H2 partial pressure and the SMA based on propionate andbutyrate as the substrates. A clear correlation was found between H2 partial pressureand the degradation rates of propionate and butyrate. The decrease in H2 partialpressure can accelerate the degradation rates of propionate (A) and butyrate (B).

    J. BIOSCI. BIOENG.,for syntrophic bacteria responsible for degrading intermediateVFAs, including propionate and butyrate (2,26). In an anaerobicreactor with a relatively high sludge HUR, the H2 partial pressurewill be maintained at a low level. As illustrated in Fig. 3, the H2partial pressure of the system used in the present study wasreduced as HUR increased sequentially from CSTR to UASB1, andthen to ASB2.

    However, the data of UASB2, UASB3 and UASB4 in Fig. 3 alsoshows that the lack of H2 partial pressure results in the decrease ofsludge HUR sequentially. This nding is in contrast to theassumption that an anaerobic digester with a lower H2 partialpressure has greater sludge HUR. A possible explanation for thesecontradictory results is that increasing H2 concentration, as anavailable substrate for hydrogenotrophic methanogens, signi-cantly favours the metabolism of these species. However, if H2partial pressure is alwaysmaintained at an extremely low level for asteady operating system, then the metabolism and growth of thehydrogenotrophic methanogens will be inhibited in a certain de-gree because of the low substrate concentration, thus resulting in arelatively low activity of the species.

    0

    20

    40

    60

    80

    100

    CSTR UASB1 UASB2 UASB3 UASB4

    H2

    parti

    al p

    ress

    ure

    (P

    a)

    0.0

    0.5

    1.0

    1.5

    2.0

    2.5

    3.0

    3.5

    HU

    R (g

    COD/

    (gVSS

    d))

    H2 partial pressure HUR

    FIG. 3. Relationship between HUR and H2 partial pressure in different AD process. H2partial pressure will be maintained at a low level if an anaerobic reactor possesses arelatively high sludge HUR; But if the H2 partial pressure always maintained at anextremely low level, then the metabolism and growth of the hydrogenotrophicmethanogens will be inhibited because of the low substrate concentration, thusresulting in a relative low activity of this species.

    522 HOU ET AL.Effects of H2 partial pressure on SMA-propionate and SMA-butyrate By monitoring H2 partial pressure in ve anaerobicreactors, a clear correlation was found between H2 partial pressureand the degradation rates of propionate and butyrate (Fig. 4). Thedecrease in H2 partial pressure can accelerate the degradationrates of propionate and butyrate. This experimental result is inaccordance with theoretical thermodynamic considerations,which indicate that because the oxidation of propionate andbutyrate has a positive Gibbs free energy (6G), the degradationof propionate and butyrate is possible only when degradationproducts, particularly H2, are effectively removed by themethanogens.

    A relatively low H2 partial pressure can result in higher degra-dation rates for propionate and butyrate, namely, SMA-propionateand SMA-butyrate. Combining with the results of Fig. 3 that H2partial pressure can be maintained at a low level if the sludge HURis relatively high in an anaerobic reactor, then it can be concludedthat the degradation rates of propionate and butyrate can beimproved by improving HUR of sludge to ensure that the anaerobicdigester will operate efciently.

    Relationship between HUR and total specic methanogenicactivity Total specic methanogenic activity (TSMA) is denedas the sum of the specic methanogenic activities against acetate(SMA-acetate) and H2/CO2 (SMA-H2/CO2). A linear increase in TSMA0

    20

    40

    60

    80

    0.0

    0.2

    0.4

    0.6

    SMA

    -but

    yrat

    e (g

    COD/

    (gVSS

    d

    H2

    parti

    al p

    ress

    ure

    (Pa)

    thus enhancing system stability.In conclusion, a higher HUR of sludge indicates more benets for

    propionate and butyrate degradation, thus resulting in improve-ments in the methanogenic activity of anaerobic microorganism.

    y = 1.2069x + 0.5395R2 = 0.9232

    0.0

    1.0

    2.0

    3.0

    4.0

    5.0

    0.0 0.5 1.0 1.5 2.0 2.5 3.0

    HUR (gCOD/(gVSSd)

    TSM

    A (gC

    OD/(g

    VSSd

    )

    FIG. 5. Positive correlation between HUR and TSMA. A linear increase in TSMA wasobserved as HUR test value increased from 0.97 gCOD/(gVSS$ d) to 2.46 gCOD/(gVSS$d). This result suggests that a higher HUR of sludge indicates more benets for pro-pionate and butyrate degradation; thereby the methanogenic activity of anaerobicmicroorganism will be stimulated.

  • HUR can therefore be used as a key parameter for evaluating andmonitoring the performance of anaerobic processes.

    ACKNOWLEDGMENT

    The study was nancially supported by a grant from the Na-tional Natural Science Foundation of China (Grant no. 50878178).

    References

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    5. Frigon, J.-C. and Guiot, S. R.: Impact of liquid-to-gas hydrogen mass transferon substrate conversion efciency of an upow anaerobic sludge bed and lterreactor, Enzyme Microb. Technol., 17, 1080e1086 (1995).

    6. McInerney, M. J., Bryant, M. P., and Stafford, D. A.: Metabolic stages andenergetics of microbial anaerobic digestion, pp. 91e97, in: Stafford, D. A.,Wheatley, B. I., and Hudges, D. E. (Eds.), Anaerobic digestion. Applied SciencePublishers, London (1980).

    13. Lee, J. C., Kim, J. H., Chang, W. S., and Pak, D.: Biological conversion of CO2 toCH4 using hydrogenotrophic methanogen in a xed bed reactor, Chem. Tech-nol. Biotechnol., 87, 844e847 (2012).

    14. Schmidt, J. E. and Ahring, B. K.: Effects of hydrogen and formate on thedegradation of propionate and butyrate in thermophilic granules from anupow anaerobic sludge blanket reactor, Appl. Environ. Microbiol., 59,2546e2551 (1993).

    15. Jeon, B. Y., Kim, S. Y., Park, Y. K., and DH, P.: Enrichment of hydrogenotrophicmethanogens in coupling with methane production using an electrochemicalbioreactor, J. Microbiol. Biotechnol., 19, 1665e1671 (2009).

    16. Lebo, A. I., Netrusov, A. I., and Conrad, R.: Effect of hydrogen concentration onthe hydrogenotrophic methanogenic community structure studied by T-RELPanalysis of 16S rRNA gene amplicons, Microbiology, 75, 786e791 (2006).

    17. Demirel, B. and Scherer, P.: The roles of acetotrophic and hydrogenotrophicmethanogens during anaerobic conversion of biomass to methane: a review,Environ. Sci. Bio/Technol., 7, 173e190 (2008).

    18. Gijzen, H. J., Bernal, E., and Ferrer, Henry: Cyanide toxicity and cyanidedegradation in anaerobic wastewater treatment, Water Res., 34, 2447e2454(2000).

    19. Leu, J.-Y., Lin, Y.-H., and Chang, F.-L.: Conversion of CO2 into CH4 by methane-producing bacterium FJ10 under a pressurized condition, Chem. Eng. Res.Desig., 89, 1879e1890 (2011).

    20. Coates, John D., Coughlanb, M. F., and Colleranb, E.: Simple method for themeasurement of the hydrogenotrophic methanogenic activity of anaerobicsludges, J. Microbiol. Methods, 26, 237e246 (1996).

    21. Luo, G. and Angelidaki, I.: Integrated biogas upgrading and hydrogen utili-zation in an anaerobic reactor containing enriched hydrogenotrophic meth-anogenic culture, Biotechnol. Bioeng., 109, 2729e2736 (2012).

    22. APHA: Standard methods for the examination of water and wastewater, 20thed. American Publish Health Association/American Water Work Association/Water Environment Federation, Washington, D.C. (1998).

    VOL. 117, 2014 SIGNIFICANCE OF HUR FOR EVALUATING AD PROCESS 5237. McCarty, P. L. and Smith, D. P.: Anaerobic wastewater treatment, Environ. Sci.Technol., 20, 1200e1206 (1986).

    8. Fynn, G. and Syala, M.: Hydrogen regulation of acetogenesis from glucose byfreely suspended and immobilised acidogenic cells in continuous culture,Biotechnol. Lett., 12, 621e626 (1990).

    9. Ligthart, Jos and Nieman, Hans: Workshop on harmonisation of anaerobicbiodegradation activity and inhibition assays, pp. 1e10. Institute for Environ-ment and Sustainability, Ispra, Italy (2002).

    10. Christensen, T. H., Bjerg, P. L., Banwart, S. A., Jakobsen, R., Heron, G., andAlbrechtsen, H.-J.: Characterization of redox conditions in groundwatercontaminant plumes, J. Contam. Hydrol., 45, 165e241 (2000).

    11. Smith, P. H. and Mah, R. A.: Kinetics of acetate metabolism during sludgedigestion, Appl. Microbiol., 14, 368e371 (1966).

    12. Garcia, J.-L., Patel, B. K. C., and Ollivier, B.: Taxonomic, phylogenetic, andecological diversity of methanogenic archaea, Anaerobe, 6, 205e226 (2000).23. Pauss, A., Andre, G., Perrier, M., and Guiot, S. R.: Liquid-to-gas mass transferin anaerobic processes: inevitable transfer limitations of methane andhydrogen in the biomethanation process, Appl. Environ. Microbiol., 56,1636e1644 (1990).

    24. Bagi, Z., Acs, N., Balint, B., Horvath, L., Dobo, K., Perei, K. R., Rakhely, G., andKovacs, K. L.: Biotechnological intensication of biogas production, Appl.Microbiol. Biotechnol., 76, 473e482 (2007).

    25. Sez-Navarrete, C., Rodrguez-Crdova, L., Baraza, X., Gelmi, C., andHerrera, L.: Hydrogen kinetics limitation of an autotrophic sulphate reductionreactor, DYNA-Colombia, 79, 126e132 (2012).

    26. Rozzi, A. and Remigi, E.:Methods of assessing microbial activity and inhibitionunder anaerobic conditions: a literature review, Environ. Sci. Bio/Technol., 3,93e115 (2004).

    Hydrogen utilization rate: A crucial indicator for anaerobic digestion process evaluation and monitoringMaterials and methodsSludge samplesThe experimental HUR test deviceHUR test procedureHUR calculationGas analysesSMA test

    Results and discussionOptimization of assay conditionRelationship between H2 partial pressure and HUREffects of H2 partial pressure on SMA-propionate and SMA-butyrateRelationship between HUR and total specific methanogenic activity

    AcknowledgmentReferences

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