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A model describing the interactions between anaerobic microbiology and geochemistry in a soil amended with glucose and nitrate

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A model describing the interactions between anaerobic microbiology and geochemistry in a soil amended with glucose and nitrate
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  A modeldescribing the interactionsbetween anaerobicmicrobiologyand geochemistry in a soil amendedwithglucose and nitrate F. D ASSONVILLE a , P. R ENAULT a & V. V ALLE ` S b a Unite´  ‘‘Climat, Sol et Environnement’’, INRA, Domaine Saint-Paul, Site Agroparc, 84914 Avignon Cedex 9, and   b Laboratoire deChimie et Environnement, Case 29, Universite´  de Provence (Aix-Marseille 1), 3 place Victor Hugo, 13331 Marseille Cedex 3, France Summary Under anaerobic conditions, microbes closely interact with geochemical reactions and can have animpact on the soil, the deep vadose zone, the underlying aquifer and the atmosphere. We have designeda model combining anaerobic microbial activities with geochemical reactions in the soil, and assessed it inbatch experiments. The model describes the dynamics of six functional microbial communities, theirdecomposition after death, and the catabolism of carbohydrates through denitrification, dissimilatoryNH 4 þ production, Fe(III) reduction, fermentation, acetogenesis, and SO 42–  reduction. It was combinedwith a model that thermodynamically describes acid–base, reduction–oxidation and complexation reac-tions in solution, and kinetic precipitation and dissolution. Batch incubations were done on a CalcicCambisol, either without amendment, or after supplying (i) glucose or (ii) glucose and NO 3 –  . Gases,mineral cations and anions, glucose, fatty acids and alcohols were measured during incubation. Netproduction of CO 2  was similar for both glucose treatments, about 40 times larger than in the control. Forthe glucose treatments, the main microbial activities were fermentation, acetogenic transformation of ethanol, and oxidation of H 2 . When the soil was enriched with NO 3 –  , no H 2  was produced, and microbialactivities were rapidly inhibited by NO 2 –  . The model shows these trends as well as geochemical char-acteristics including pH and reduction–oxidation potential. Introduction Anaerobic conditions prevail in flooded soils, and in organic-rich soils when a transient excess of moisture occurs. Theyaffect soil functions, the underlying aquifers and the atmo-sphere. Undesirable effects of anaerobiosis include metalmobilization, accumulation of toxic products (e.g. acetate,propionate, NO 2 –  ), and the emission of greenhouse gases.Beneficial effects include the reduction of NO 3 –  and conse-quent diminution of pollution (Casella & Payne, 1996), thedegradation of organic contaminants, and the immobilizationof some toxic metals and radionuclides (Lovley, 1995).Anaerobic microbial activities are closely linked to geo-chemical reactions. Microbial activities affect (i) pH, via netmicrobial output of H þ , CO 2 , NH 4 þ , HS  –  and organic acids(Stumm & Morgan, 1996), (ii) the soil’s redox potential, byinfluencing redox couples including NO 3 –  and NO 2 –  , Fe 3 þ andFe 2 þ , H þ and H 2 , SO 42–  and HS  –  , CO 2  and CH 4  (Peters &Conrad, 1996), (iii) the amount of complexing organic acids(Glissman & Conrad, 2000), and (iv) the alteration of solidparticles (Stumm & Morgan, 1996). Geochemical characteris-tics affect (i) availability of substrate for microorganisms, (ii)the thermodynamic feasibility of reactions, e.g. H 2  may repressacetogen transformations (Schink, 1997), and (iii) inhibitions(NO 2 –  and undissociated volatile fatty acids). Microbiallyinduced changes may be partly buffered by dissolution of calcite and metal oxide, and the precipitation of other minerals(Stumm & Morgan, 1996). Geochemical transformations maypartly regenerate some microbial substrates, e.g. the chemicaloxidation of HS  –  to S 0 with the concomitant reduction of Fe 3 þ to Fe 2 þ (Murase & Kimura, 1997).The main anaerobic microbial activities in the soil have beenmuch studied through (i) the reduction of various terminalelectron acceptors during respiratory processes, including N,Mn, Fe and S oxides (Widdel, 1988; Pelmont, 1993; Lovley,1995), (ii) fermentation and acetogenic reactions (Stams, 1994),and (iii) methanogenesis (Oremland, 1988). So far, only afew studies have focused on lipid and protein degradation Correspondence: F. Dassonville.E-mail: fabrice.dassonville@avignon.inra.frReceived 10 December 2002; revised version accepted 1 July 2003 European Journal of Soil Science , March 2004,  55,  29–45 doi: 10.1046/j.1365-2389.2004.00594.x #  2004 Blackwell Publishing Ltd  29  (Finnerty, 1989; Jones, 1999). Recently, the use of molecularbiology techniques has improved the description of the diversityand structure of microbial consortia (Head  etal  ., 1998). Geo-chemical reactions are generally well characterized. However,their descriptions remain inadequate for (i) the solid and solutespeciations of some compounds, including Fe (Brown  etal  .,1999), (ii) the kinetics between solid particles and solution(Stumm & Morgan, 1996), and (iii) the properties of organicligands that vary with the soil.Only a few soil models combine microbial activities andgeochemical reactions (Dassonville & Renault, 2002); in thesecases, geochemistry is reduced to acid–base reactions (Vavilin etal  ., 2000). Several models have been proposed for otheranaerobic environments, including the deep vadose zone andaquifers, anaerobic waste digesters, and the rumens of cattle(Dassonville & Renault, 2002). Microbial communities in thesoil are specific, models established for rumens and digestersignore the biogeochemical interactions between solid particlesand solution, which prevail in soils, and models established forthe aquifer do not accurately describe microbial activities,while they account for geochemical reactions that are notalways predominant in the soil.We have developed a new model combining microbial andgeochemical transformations to describe the environmentaleffects of transient anaerobic events in the soil, and assessedthis model on batch incubations performed on a soil supple-mented with an electron donor (glucose), and an electronacceptor (NO 3 –  ). We describe it below. Modelling anaerobic biogeochemical transformations Functional microbial communities The model accounts for six functional microbial communitiesclassified according to their catabolic activities (Dassonville &Renault, 2002) (Table 1): denitrifiers (Pelmont, 1993), Fe redu-cers (Lovley, 1995), two fermentative communities producingeither acetate and ethanol, or butyrate (Pelmont, 1993), aceto-gens (Dolfing, 1988), and SO 42–  reducers (Widdel, 1988). Microbial activities Each functional community attempts to meet its optimumenergy requirement through one or more metabolic pathways(Table 1). A metabolic pathway is a subset of catabolic activ-ities among 14 possibilities (Table 2) that compete with oneanother for substrate. Microbial communities that can exploitmore than one pathway use first those that are more efficientenergetically, and may then use other pathways to minimizethe difference between their optimum requirement and theenergy supplied. Some pathways that contribute poorly toenergy supply are always activated: these are formate lysisand formate oxidation.The actual rates  V   j   (mol kg  1 soil s  1 ) of activities  j   areproportional to the biomass of the microbial community  i   thatperforms the transformation: V   j   ¼  m i     v  j  ;  ð 1 Þ where  v  j   is the specific rate of activity  j   (mol g  1 biomass s  1 ),and  m i   is the microbial biomass  i   that performs reaction  j   (gkg  1 soil). Specific rates depend on the amounts of mineral N.When shortage of N does not limit microbial growth, thepotential specific rate  v  j  p  of reaction  j   is described by aMichaelis–Menten type formalism. For respiratory activities,the model assumes v  j  p  ¼  v  j  max S  a ½  S  a ½  þ  K  m  j  a    S  d ½  S  d ½  þ  K  m  j  d    f  e ;  ð 2a Þ where  v  j  max  is the maximum rate of specific activity  j   (mol g  1 s  1 ), [ S  a ] and [ S  d ] are the concentrations of the electron accep-tor and donor (mol l  1 ), respectively,  K  m  j  a  and  K  m  j  d  are theMichaelis constants for the electron acceptor and donor (moll  1 ), respectively, and  f  e  is a dimensionless function thatdescribes environmental effects other than competitionbetween substrates. For non-respiratory activities (lysis, fer-mentations, and acetogenic activities), the model assumes v  j  p  ¼  v  j   max S  s ½  S  s ½  þ  K  m  js    f  e ;  ð 2b Þ where  s  is the index of the substrate concerned. When there iscompetition between substrates for the same metabolic path-ways (e.g. NO 3 –  , NO 2 –  and N 2 O during glucose oxidation),Michaelis constants  K  m  js  of the activities concerned arereplaced by an effective Michaelis constant  K  0 m  js  (mol l  1 )for substrate  s  such that K  0 m  js  ¼  K  m  js  1 þ X s 0 6¼ s S  s 0 ½  K  m  js 0  ! :  ð 3 Þ To ensure the uniqueness of the optimal electron flux requiredfor the microorganisms concerned, maximum rates of compet-ing catabolic activities simultaneously verify v  j   max  ¼  n e  j  0 n e  j  v  j  0 max 8  j  ;  ð 4 Þ where n e  j   and n e  j  0  are the numbers of   e  –  exchanged duringrespiratory activities  j   and  j  0 .The environmental function  f  e  is either one elementary func-tion between 0 and 1, or the product of several such functions.It describes the following. 1  The inhibition by NO 2 –  (  f  eNO2 –  ) (Klu ¨ber & Conrad, 1998),on the assumption that  f  eNO2 –  equals 0 when the concentrationof NO 2 –  in solution exceeds 4m M , and 0.5 at 5m M . 2  The effect of pH (  f  epH ) on formate lysis or oxidation, andN 2 O reduction. As regards formate,  f  epH ¼ 1 at pH < 6, 0 atpH > 7.7, and varies linearly between these pH (Pelmont, 30  F. Dassonville  et al. # 2004 Blackwell Publishing Ltd,  European Journal of Soil Science ,  55,  29–45  1993). As regards N 2 O,  f  epH ¼ 0 at pH <  6 and 1 at pH > 7.5,and it varies linearly between these values (Holtan-Hartwig etal  ., 2000). 3  The effect of H 2  partial pressure on acetogenic activities(  f  eH2 ). When the Gibbs’ free energy,   G , of these activities ispositive (i.e. endergonic reaction), acetogenic activity is notpossible. When   G  is negative but not sufficient to ensurethe production of one ATP coupled to the excretion of 3H þ (across the membrane) the rate of activity is reduced and isproportional to   G . We assumed that 1ATP synthesisrequires 70kJ (Schink, 1997). Microbial dynamics Microbial growth and death result from the balance betweenthe energy supplied by catabolism and the energy required formaintenance. For non-limiting N, the balance is b i  p  ¼  m i  X  j  ð v  j  p    Y  max  j     Y  m Þ  !   m E i  ( ) ;  ð 5 Þ where  b i  p  is the energy balance expressed as an equivalentgenerated biomass  i   (g kg  1 soil s  1 ),  Y  max  j   is the maximumyield of reaction  j   when maintenance requirements can beignored (mol ATP mol  1 substrate) (Table 2),  m E i   is therequirement for microbial maintenance (s  1 ), and  Y  m  is themicrobial biomass accumulated per ATP consumed (g mol  1 ATP) (Pelmont, 1993). The last,  Y  m , was equal to 12 and6.5gmol  1 for heterotrophs and autotrophs, respectively(Bauchop & Elsden, 1960). When  b i  p  is positive the potentialgrowth  g i  p  of microbial community  i   is  g i  p  ¼  b i  p :  ð 6 Þ Actual microbial growth depends on the availability of N,provided that N corresponds to 10.36 %  of the biomass(Vavilin  etal  ., 1994). Nitrogen pools are used in the followingorder: NH 4 þ , NO 2 –  , NO 3 –  . We define a dimensionless function  f  N  to describe availability of N:  f  N  ¼  g i  a  g i  p ;  ð 7 Þ where  g i  a  is the actual growth (g kg  1 soil). Actual specificrates  v  j   of reactions  j   are then expressed as v  j   ¼  v  j  p    v  j  p m E i  P  j  0 6¼  j  v  j  0 p Y  max  j  0 0B@1CA8><>:9>=>;  f  N ;  ð 8 Þ since shortage of N affects only microbial growth (not main-tenance), with a reduction proportional to  f  N  whichever com-munity is concerned. If the microbial composition correspondsto C 40.4 H 77.4 O 20.9 N 7.4  formula weight (Vavilin  etal  ., 1994),then the anabolic reactions (15) to (20) in Table 2 describesynthesis of biomass using the same organic substrates as forcatabolic activities. When  b i  p  is negative (i.e. no growth) themineralized fraction  F  i   of the dying biomass  d  i   balances themaintenance requirements of the surviving bacteria: d  i   ¼  b i  p F  i  ¼ m i  P v  j  p    Y  max  j     Y  m     m E i  n o F  i  :  ð 9 Þ We assume that the dead biomass is mineralized by acetateand butyrate fermentative communities according to reactions(13) and (14) in Table 2, respectively: the microbial biomass isdecomposed by carbohydrate fermentation (see above), pro-tein fermentation (Vavilin  etal  ., 1994), and    -oxidation of lipids (Vavilin  etal  ., 1994). Table1  Functional microbial communities, and relevant metabolic pathways and activitiesFunctional microbial community Metabolic pathway Activity a Denitrifying community Denitrification (1), (2), (3)FeIII reducers FeIII reduction (5)Butyric fermentative community Butyric fermentation (9)Dissimilatory NH 4 þ production (1), (4)Formate lysis (7)Formate oxidation (8)Biomass decomposition (14)Acetic fermentative community Acetic fermentation (6)Dissimilatory NH 4 þ production (1), (4)Formate lysis (7)Formate oxidation (8)Biomass decomposition (13)Acetogens Acetogenesis (10), (11)Sulphate reducing community Sulphate reduction (12) a See Table 2 for description of the microbial activities. Modelling anaerobic microbial and geochemical processes  31 #  2004 Blackwell Publishing Ltd,  European Journal of Soil Science ,  55,  29–45  Table2  Description and mathematical formalism of the model reactionsModel reactions References Environmental functions  f  e  ATP per reaction  Y  max  j   Note Catabolic reactions Denitrification(1) glucose  þ 12 NO  3  ! v ð 1 Þ 6 CO 2  þ 6 H 2 O  þ 12 NO  2  (Stouthamer, 1988)  f  eNO2 –  19 a(2) glucose  þ 12 NO  2  þ  12 H þ ! v ð 2 Þ 6 CO 2  þ  12 H 2 O þ 6 N 2 O (Stouthamer, 1988)  f  eNO2 –  19 a(3) glucose  þ 12 N 2 O  ! v ð 3 Þ 6 CO 2  þ  6 H 2 O þ 12 N 2  (Stouthamer, 1988)  f  eNO2 –  ,  f  epH  19 aNO 3 –  dissimilatory reduction(4) glucose  þ 43 NO  2  þ 83H þ þ  43H 2 O  ! v ð 4 Þ acetate þ  4 formate  þ 43NH 4 þ (Stouthamer, 1988)  f  eNO2 –  1/3 bFe(III) reduction(5) Fe 3 þ þ H 2  ! v ð 5 Þ Fe 2 þ þ H þ (Lovley, 1995)  f  eNO2 –  4Fermentation and acidogenesis(6) glucose  þ H 2 O  ! v ð 6 Þ 2 formate þ  acetate  þ ethanol (Pelmont, 1993)  f  eNO2 –  3(7) formate  ! v ð 7 Þ CO 2  þ H 2  (Pelmont, 1993)  f  eNO2 –  ,  f  eNO3 –  ,  f  epH  2/3(8) formate  þ NO  3  ! v ð 8 Þ CO 2  þ NO  2  þ  H 2 O (Pelmont, 1993)  f  eNO2 –  1(9) glucose  ! v ð 9 Þ butyrate þ 2 formate (Pelmont, 1993)  f  eNO2 –  3Acetogenesis(10) butyrate þ 2 H 2 O  ! v ð 10 Þ 2 acetate þ  2 H 2  (Schink, 1997)  f  eNO2 –  ,  f  eH2  4/3 c(11) ethanol  þ H 2 O  ! v ð 11 Þ acetate  þ 2 H 2  (Schink, 1997)  f  eNO2 –  ,  f  e 0 H2  4/3 cSO 42–  reduction(12) H 2  þ 14SO 2  4  þ 12H þ ! v ð 12 Þ  14H 2 S þ  H 2 O (Widdel, 1988)  f  eNO2 –  1/2 dDecomposition of dead biomass(13) C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 19 : 5 H 2 O  ! v ð 13 Þ 18 : 5 acetate  þ 6 : 7 H 2  þ  0 : 8 ethanol þ  1 : 7 formate þ  7 : 4 NH 3  f  eNO2 –  20 e(14) C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 8 H 2  þ 4 : 7 H 2 O  ! v ð 14 Þ 8 : 2 butyrate þ  2 : 9 acetate  þ 1 : 7 formate  þ 7 : 4 NH 3  f  eNO2 –  20 e  3  2   F  .D a s  s  o n v  i   l   l   e   e  t   al     .  # 2   0   0  4  B l     a c k   w e l    l    P  u b  l    i     s h  i    n  gL  t   d    , E ur  o p e  a n J  o ur  n a l   o f   S  o i   l   S  c  i   e  n c  e    ,  5   5    , 2   9  –4   5    Anabolic reactions (15) 6 : 73 glucose þ 7 : 4 NH 3  ! v ð 15 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 12 : 8 H 2 O  f  eNO2 –  f (16) 20 : 2 ethanol þ 7 : 4 NH 3  ! v ð 16 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ  20 : 2 H 2 O  f  eNO2 –  f (17) 40 : 4 formate þ  7 : 4 NH 3  ! v ð 17 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 12 : 8 H 2 O  f  eNO2 –  f (18) 10 : 1 butyrate þ  7 : 4 NH 3  ! v ð 18 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 0 : 7 H 2 O  f  eNO2 –  f (19) 20 : 2 acetate þ  7 : 4 NH 3  ! v ð 19 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 12 : 8 H 2 O  f  eNO2 –  f (20) 40 : 4 CO 2  þ  7 : 4 NH 3  þ  87 : 3 H 2  ! v ð 20 Þ C 40 : 4 H 77 : 4 O 20 : 9 N 7 : 4  þ 59 : 9 H 2 O  f  eNO2 –  f  a Assuming that energy from denitrification represents 50 % of that obtained from O 2  respiration. b Minimum supplied by microbial activity corresponding to one proton excreted (Schink, 1997). c Assuming that the translocation of 3H þ from the outside to the cytoplasm is combined with the formation of 1ATP. d The reduction of 1mol SO 42–  produces 3ATP, but 1ATP is consumed to activate SO 42–  before (Widdel, 1988; Pelmont, 1993). e The energy gain corresponds to the fermentation of carbohydrate in dead biomass, assuming the amount of ATP provided per C of dead biomass. f  Assuming that the C substrates for catabolic and anabolic reactions are the same, the efficiencies  e S  of substrates S are 1.86, 1.21, 0.93, 0.89, 1.21 and 0.48g substrate consumed throughanabolic pathways per g of biomass synthesized, for formate, acetate, ethanol, butyrate, glucose and CO 2 , respectively. Reactions are not equilibrated for O and N components. M o d  e  l   l   i   n g a n a e r  o b  i   c  m i   c r  o b  i   a l   a n d  g e  o c  h  e  m i   c  a l   pr  o c  e  s  s  e  s   3   3    # 2   0   0  4  B l     a c k   w e l    l    P  u b  l    i     s h  i    n  gL  t   d    , E ur  o p e  a n J  o ur  n a l   o f   S  o i   l   S  c  i   e  n c  e    ,  5   5    , 2   9  –4   5  
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