Skip to main content

Advertisement

SpringerLink
Log in

pH shift-mediated dehydrogenation and hydrogen production are responsible for microbial iron(III) reduction in submerged paddy soils

  • Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

An Erratum to this article was published on 16 April 2015

Abstract

Purpose

pH shift-induced responses of iron(III) [Fe(III)] reduction and associated dehydrogenation and hydrogen (H2) production in submerged paddy soils were investigated to improve our understanding of the contribution of fermentative processes to microbial Fe(III) reduction.

Materials and methods

A 40-day anaerobic incubation experiment was conducted using two paddy soils from geographically distinct regions in northern (Hapli-Stagnic Anthosol, HSA; pH 8.14) and southern China (Fe-accumili-Stagnic Anthosol, FSA; pH 5.00), respectively. The initial soil pH was adjusted with aluminum sulfate or sodium carbonate to strongly acidic, acidic, neutral, alkaline, and strongly alkaline levels.

Results and discussion

During anaerobic incubation, as the initial soil pH shifts to acidic or lower levels, dehydrogenase activity (DHA) was greatly inhibited. However, increased acid-soluble Fe(III) level was accompanied by decreased maximum Fe(III) reduction potential (a) and prolonged time to maximum Fe(III) reduction rate (T Vmax ). Decreased pH led to a significantly lower peak partial pressure of H2 (ppH 2max ) in HSA and an increase in FSA. The initial shifts in pH to neutral and higher levels had no significant effect on DHA or acid-soluble Fe(III); however, ppH 2max declined in the neutral treatment of HSA, while T Vmax decreased slightly in the presence of a low ppH2 in the neutral to strongly alkaline FSA. DHA was correlated with Fe(II) accumulation in both paddy soils during the rapid Fe(III) reduction stage (p < 0.05).

Conclusions

DHA is related to microbially mediated Fe(III) reduction in anaerobic paddy soils. pH shift-mediated enzymatic dehydrogenation and fermentative H2 production are responsible for microbial Fe(III) reduction in flooded rice fields, with initial pH as the main driving force.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

Fe(III):

Iron(III)

Fe oxides:

Fe (oxyhydr)oxides

DHA:

Dehydrogenase activity

HSA:

Hapli-Stagnic Anthrosol

FSA:

Fe-accumili-Stagnic Anthrosol

ppH2 :

Partial pressure of H2

V max :

Maximum Fe(III) reduction rate

T Vmax :

Time to maximum Fe(III) reduction rate

DHA max :

Maximum dehydrogenase activity

T DHAmax :

Time to maximum dehydrogenase activity

ppH 2max :

Peak of hydrogen partial pressure

T ppH2max :

Time to peak of hydrogen partial pressure

pH i :

Initial soil pH

CCA:

Canonical correspondence analysis

References

  • Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72

    Article  CAS  Google Scholar 

  • Balashova V, Zavarzin G (1979) Anaerobic reduction of ferric iron by hydrogen bacteria. Microbiology 48:773–778

    CAS  Google Scholar 

  • Blothe M, Akob DM, Kostka JE, Goschel K, Drake HL, Kusel K (2008) pH gradient-induced heterogeneity of Fe(III)-reducing microorganisms in coal mining-associated lake sediments. Appl Environ Microbiol 74:1019–1029

    Article  Google Scholar 

  • Bonneville S, Cappellen PV, Behrends T (2004) Microbial reduction of iron(III) oxyhydroxides: effects of mineral solubility and availability. Chem Geol 212:255–268

    Article  CAS  Google Scholar 

  • Braak CJE, Verdonschot PEM (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquat Sci 57:255–289

    Article  Google Scholar 

  • Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234

    Article  CAS  Google Scholar 

  • Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soil and sediments. FEMS Microbiol Ecol 28:193–202

    Article  CAS  Google Scholar 

  • Detkova EN, Pusheva MA (2006) Energy metabolism in halophilic and alkaliphilic acetogenic bacteria. Microbiology 75:1–11

    Article  CAS  Google Scholar 

  • Dick WA, Tabatabai MA (1992) Significance and potential uses of soil enzymes. In: Metting FB Jr (ed) Soil microbial ecology: applications in agricultural and environmental management. Marcel Dekker Inc., New York, pp 95–127

    Google Scholar 

  • Garrels RM, Christ CL (1965) Solutions minerals and equilibria. In: Garrels RM, Christ CL (eds) Happer & Roy: New York, Evanstan & London. John Weatherhell, Inc., Tokyo

  • Grybos M, Davranche M, Gruau G, Petitjean P, Pédrot M (2009) Increasing pH drives organic matter solubilization from wetland soils under reducing conditions. Geoderma 154:13–19

    Article  CAS  Google Scholar 

  • Guan SY (1986) Soil enzyme research method. China Agriculture Press, Beijing (in Chinese)

    Google Scholar 

  • He JZ, Qu D (2008) Dissimilatory Fe(III) reduction characteristics of paddy soil extract cultures treated with glucose or fatty acids. J Environ Sci 20:1103–1108

    Article  CAS  Google Scholar 

  • Hori T, Muller A, Igarashi Y, Conrad R, Friedrich MW (2009) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4:267–278

    Article  Google Scholar 

  • Hoy CW, Grewal PS, Lawrence JL, Jagdale G, Acosta N (2008) Canonical correspondence analysis demonstrates unique soil conditions for entomopathogenic nematode species compared with other free-living nematode species. Biol Control 46:371–379

    Article  CAS  Google Scholar 

  • Jaeckel U, Schnell S (2000) Suppression of methane emission from rice paddies by ferric iron fertilization. Soil Biol Biochem 32:1811–1814

    Article  Google Scholar 

  • Jia R, Yi WJ, Qu D (2012) Study on influencing factors for TTC-dehydrogenase activity measurement in slurry of paddy soil. Acta Agric Boreali-Occidentalis Sin China 21:154–158 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Jiang L, Zhu J, Wang H, Fu Q, Hu H, Huang Q, Violante A, Huang L (2014) Sorption of humic acid on Fe oxides, bacteria, and Fe oxide-bacteria composites. J Soils Sediments 14:1378–1384

    Article  CAS  Google Scholar 

  • Kizilkaya R (2008) Dehydrogenase activity in Lumbricus terrestris casts and surrounding soil affected by addition of different organic wastes and Zn. Bioresour Technol 99:946–953

    Article  CAS  Google Scholar 

  • Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14

    Article  Google Scholar 

  • Kwon MJ, Boyanov MI, Antonopoulos DA, Brulc JM, Johnston ER, Skinner KA, Kemner KM, O’Loughlin EJ (2014) Effects of dissimilatory sulfate reduction on FeIII (hydr)oxide reduction and microbial community development. Geochim Cosmochim Acta 129:177–190

    Article  CAS  Google Scholar 

  • Lan Y, Yang J, Deng B (2006) Catalysis of dissolved and adsorbed iron in soil suspension for chromium(VI) reduction by sulfide. Pedosphere 16:572–578

    Article  CAS  Google Scholar 

  • Laura RD (1976) Effects of alkali salts on carbon and nitrogen mineralization of organic matter in soil. Plant Soil 44:587–596

    Article  CAS  Google Scholar 

  • Lefort S, Mucci A, Sundby B (2012) Sediment response to 25 years of persistent hypoxia. Aquat Geochem 18:461–474

    Article  CAS  Google Scholar 

  • Lehours AC, Evans P, Bardot C, Joblin K, Gerard F (2007) Phylogenetic diversity of archaea and bacteria in the anoxic zone of a meromictic lake (Lake Pavin, France). Appl Environ Microbiol 73:2016–2019

    Article  CAS  Google Scholar 

  • Lehours AC, Batisson I, Guedon A, Mailhot G, Fonty G (2009) Diversity of culturable bacteria, from the anaerobic zone of the meromictic Lake Pavin, able to perform dissimilatory-iron reduction in different in vitro conditions. Geomicrobiol J 26:212–223

    Article  CAS  Google Scholar 

  • Lehtovirta LE, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota. FEMS Microbiol Ecol 70:367–376

    Article  CAS  Google Scholar 

  • Lentini CJ, Wankel SD, Hansel CM (2012) Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol 3:1–19

    Article  Google Scholar 

  • Li Q (2012) Enrichment of phosphate on ferrous iron phases during bio-reduction of ferrihydrite. Int J Geosci 3:314–320

    Article  CAS  Google Scholar 

  • Li FB, Li XM, Zhou SG, Zhuang L, Cao F, Huang DY, Xu W, Liu TX, Feng CH (2010) Enhanced reductive dechlorination of DDT in an anaerobic system of dissimilatory iron-reducing bacteria and iron oxide. Environ Pollut 158:1733–1740

    Article  CAS  Google Scholar 

  • Li HJ, Peng JJ, Weber KA, Zhu YG (2011) Phylogenetic diversity of Fe(III)-reducing microorganisms in rice paddy soil: enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sediments 11:1234–1242

    Article  CAS  Google Scholar 

  • Lovley DR (1987) Organic matter mineralization with the reduction of ferric iron: a review. Geomicrobiol J 5:375–399

    Article  CAS  Google Scholar 

  • Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287

    CAS  Google Scholar 

  • Lovley DR (2006) Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. In: Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, Dworkin M (eds) The prokaryotes. Springer, New York, pp 635–658

    Chapter  Google Scholar 

  • Lovley DR, Philips EJP (1987) Competitive mechanisms for inhibition of sulfate reduction and methane production in the zone of ferric iron reduction in sediments. Appl Environ Microbiol 53:2636–2641

    CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689

    CAS  Google Scholar 

  • Maeda T, Sanchez-Torres V, Wood TK (2007) Escherichia coli hydrogenase-3 is a reversible enzyme possessing hydrogen uptake and synthesis activities. Appl Microbiol Biotechnol 76:1035–1042

    Article  CAS  Google Scholar 

  • McLaren AD, Peterson GH (1967) Soil biochemistry. Marcel Dekker, New York

    Google Scholar 

  • Menon P, Gopal M, Parsad R (2005) Effects of chlorpyrifos and quinalphos on dehydrogenase activities and reduction of Fe3+ in the soils of two semi-arid fields of tropical India. Agric Ecosyst Environ 108:73–83

    Article  CAS  Google Scholar 

  • Nicol GW, Webster G, Glover LA, Prosser JI (2004) Differential response of archaeal and bacterial communities to nitrogen inputs and pH changes in upland pasture rhizosphere soil. Environ Microbiol 6:861–867

    Article  CAS  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The Influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  CAS  Google Scholar 

  • Noguchi K, Riggins DP, Eldahan KC, Kitko RD, Slonczewski JL (2010) Hydrogenase-3 contributes to anaerobic acid resistance of Escherichia coli. PLoS One 5:10132–10138

    Article  Google Scholar 

  • Page AL, Miller RH, Keeny OR (1982) In: Buxton DR (ed) Chemical and microbiological properties. Methods of soil analysis, 2nd edn. American Society of Agronomy Press, Madison

    Google Scholar 

  • Peter Mayer H, Conrad R (1990) Factors influencing the population of methanogenic bacteria and the initiation of methane production upon flooding of paddy soil. FEMS Microbiol Lett 73:103–111

    Article  Google Scholar 

  • Piña RG, Cervantes C (1996) Microbial interactions with aluminium. Biometals 9:311–316

    Article  Google Scholar 

  • Ponnamperuma FN (1972) The chemistry of submerged soils. In: Brady NC (ed) Advances in agronomy. Academic Press, Waltham, pp 29–96

    Google Scholar 

  • Qu D, Ratering S, Schnell S (2004) Microbial reduction of weakly crystalline iron (III) oxides and suppression of methanogenesis in paddy soil. Bull Environ Contam Toxicol 72:1172–1181

    Article  CAS  Google Scholar 

  • Sahrawat KL (2003) Organic matter accumulation in submerged soils. In: Sparks DL (ed) Advances in agronomy. Academic Press, London, pp 169–201

    Google Scholar 

  • Schnell S, Ratering S (1998) Simultaneous determination of iron(III), iron(II), and manganese(II) in environmental samples by ion chromatography. Environ Sci Technol 32:1530–1537

    Article  CAS  Google Scholar 

  • Stewart DI, Burke IT, Hughes-Berry DV, Whittleston RA (2010) Microbially mediated chromate reduction in soil contaminated by highly alkaline leachate from chromium containing waste. Ecol Eng 36:211–221

    Article  Google Scholar 

  • Tan W, Liu F (2005) Adsorption and redox reactions of heavy metals on Fe-Mn nodules from Chinese soils. J Colloid Interface Sci 284:600–605

    Article  CAS  Google Scholar 

  • Thompson A, Chadwick OA, Boman S, Chorover J (2006) Colloid mobilization during soil iron redox oscillations. Environ Sci Technol 40:5743–5749

    Article  CAS  Google Scholar 

  • Thorpe CL, Morris K, Boothman C, Lloyd JR (2012) Alkaline Fe(III) reduction by a novel alkali-tolerant Serratia sp. isolated from surface sediments close to Sellafield nuclear facility, UK. FEMS Microbiol Lett 327:87–92

    Article  CAS  Google Scholar 

  • Tian Q, Chen J, Zhang H, Xiao Y (2006) Study on the modified triphenyl tetrazolium chloride-dehydrogenase activity (TTC-DHA) method in determination of bioactivity in the up-flow aerated bio-activated carbon filter. Afr J Biotechnol 5:181–188

    CAS  Google Scholar 

  • Trchounian K, Pinske C, Sawers RG, Trchounian A (2012) Characterization of Escherichia coli [NiFe]-hydrogenase distribution during fermentative growth at different pHs. Cell Biochem Biophys 62:433–440

    Article  CAS  Google Scholar 

  • Trevors JT (1984) Effect of substrate concentration, inorganic nitrogen, O2 concentration, temperature and pH on dehydrogenase activity in soil. Plant Soil 77:285–293

    Article  CAS  Google Scholar 

  • Wang X, Chen X, Yang J, Wang Z, Sun G (2009) Effect of microbial mediated iron plaque reduction on arsenic mobility in paddy soil. J Environ Sci 21:1562–1568

    Article  CAS  Google Scholar 

  • Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752–764

    Article  CAS  Google Scholar 

  • Whittleston RA, Stewart DI, Mortimer RJG, Burke IT (2013) Enhancing microbial iron reduction in hyperalkaline, chromium contaminated sediments by pH amendment. Appl Geochem 28:135–144

    Article  CAS  Google Scholar 

  • Włodarczyk T, Stępniewski W, Brzezińska M (2002) Dehydrogenase activity, redox potential, and emissions of carbon dioxide and nitrous oxide from Cambisols under flooding conditions. Biol Fertil Soils 36:200–206

    Article  Google Scholar 

  • Włodarczyk T, Brzezińska M, Szarlip P (2005) Some physical factors influencing the dehydrogenase activity in soils (a review). Review of current problems in agrophysics Institute of Agrophysics. PAS, Lublin, pp 488–490

    Google Scholar 

  • Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, Yang Y, Yao T, Knight R, Chu H (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Microbiol 14:2457–2466

    Article  CAS  Google Scholar 

  • Xu Y, He Y, Feng X, Liang L, Xu J, Brookes PC, Wu J (2013) Enhanced abiotic and biotic contributions to dechlorination of pentachlorophenol during Fe(III) reduction by an iron-reducing bacterium Clostridium beijerinckii Z. Sci Total Environ 473–474:215–223

    Google Scholar 

  • Yang H, Shen J (2006) Effect of ferrous iron concentration on anaerobic bio-hydrogen production from soluble starch. Int J Hydrog Energy 31:2137–2146

    Article  CAS  Google Scholar 

  • Yi WJ, Wang BL, Qu D (2012) Diversity of isolates performing Fe(III) reduction from paddy soil fed by different organic carbon sources. Afr J Biotechnol 11:4407–4417

    CAS  Google Scholar 

  • Yi WJ, You JH, Zhu C, Wang BL, Qu D (2013) Diversity, dynamic, and abundance of Geobacteraceae species in paddy soil following slurry incubation. Eur J Soil Biol 56:11–18

    Article  Google Scholar 

  • Zhu C (2011) Effect of environmental factors on Geobacteraceae spp. and anaeromyxobacter spp. communities in paddy soil. Northwest Agricuture & Forest University, Yangling, in Chinese with English abstract

    Google Scholar 

  • Zhu C, Xia SH, Wang BL, Qu D (2011) Variation of Anaeromyxobacter community structure and abundance in paddy soil slurry over flooding time. Afr J Agric Res 6:6107–6118

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Natural Resources and Environment, Northwest A&F University, No. 3 Taicheng Road, Yangling, Shaanxi Province, 712100, China

    Rong Jia, Li-Na Li & Dong Qu

Authors
  1. Rong Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li-Na Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dong Qu.

Additional information

Responsible Editor: Zhenli He

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 123 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, R., Li, LN. & Qu, D. pH shift-mediated dehydrogenation and hydrogen production are responsible for microbial iron(III) reduction in submerged paddy soils. J Soils Sediments 15, 1178–1190 (2015). https://doi.org/10.1007/s11368-015-1084-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-015-1084-8

Keywords

Search

Navigation