Skip to main content

Advertisement

Springer Nature Link
Log in

Abundance and diversity of iron reducing bacteria communities in the sediments of a heavily polluted freshwater lake

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Iron reduction mediated by Fe(III)-reducing bacteria (FeRB) occurs in aqueous environments and plays an essential role in removing contaminates in polluted freshwater lakes. Two model FeRB species, Shewanella and Geobacter, have been intensively studied because of their functions in bioremediation, iron reduction, and bioelectricity production. However, the abundance and community diversity of Shewanella and Geobacter in eutrophic freshwater lakes remain largely unknown. In this work, the distribution, abundance and biodiversity of Shewanella, Geobacter and other FeRB in the sediments of a heavily polluted lake, Chaohu Lake, China, across four successive seasons were investigated. Shewanella, Geobacter, and other FeRB were found to be widely distributed in the sediment of this heavily eutrophic lake. Geobacter was abundant with at least one order of magnitude more than Shewanella in cold seasons. Three Shewanella-related operational taxonomic units were detected and sixty one Geobacter-related operational taxonomic units were grouped into three phylogenetic clades. Thiobacillus, Desulfuromonas and Geobacter were identified as the main members of FeRB in the lake sediments. Interestingly, nutrients like carbon, nitrogen, and phosphorus were found to be the key factors governing the abundance and diversity of FeRB. Total FeRB, as well as Geobacter and Shewanella, were more abundant in the heavily eutrophic zone than those in the lightly eutrophic zone. The abundance and diversity of FeRB in the sediments of freshwater lakes were highly related with the degree of eutrophication, which imply that FeRB might have a great potential in alleviating the eutrophication and contamination in aqueous environments.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

References

  • Anderson RT, Rooney-Varga JN, Gaw CV, Lovley DR (1998) Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum-contaminated aquifers. Environ Sci Technol 32:1222–1229

    Article  CAS  Google Scholar 

  • Bastviken D, Santoro AL, Marotta H, Pinho LQ, Calheiros DF, Crill P, Enrich-Prast A (2010) Methane emissions from Pantanal, South America, during the low water season: toward more comprehensive sampling. Environ Sci Technol 44:5450–5455

    Article  CAS  Google Scholar 

  • Bräuer SL, Adams C, Kranzler K, Murphy D, Xu M, Zuber P, Simon HM, Baptista AM, Tebo BM (2011) Culturable Rhodobacter and Shewanella species are abundant in estuarine turbidity maxima of the Columbia River. Environ Microbiol 13:589–603

    Article  Google Scholar 

  • Caccavo F, Blakemore RP, Lovley DR (1992) A hydrogen-oxidizing, Fe(III) reducing microorganism from the Great Bay estuary, New Hampshire. Appl Environ Microbiol 58:3211–3216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cai PJ, Xiao X, He YR, Li WW, Chu J, Wu C, He MX, Zhang Z, Sheng GP, Lam MHW, Xu F, Yu HQ (2012) Anaerobic biodecolorization mechanism of methyl orange by Shewanella oneidensis MR-1. Appl Microbiol Biotechnol 93:1769–1776

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chen M, Jiang HL (2016) Relative contribution of iron reduction to sediments organic matter mineralization in contrasting habitats of a shallow eutrophic freshwater lake. Environ Pollut 213:904–912

    Article  CAS  Google Scholar 

  • Chen X, Yang XD, Dong XH, Liu QA (2011) Nutrient dynamics linked to hydrological condition and anthropogenic nutrient loading in Chaohu Lake (Southeast China). Hydrobiologia 661:223–234

    Article  CAS  Google Scholar 

  • Coates JD, Lonergan DJ, Philips EJP, Jenter H, Lovley DR (1995) Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe (III) reducer that can oxidize long-chain fatty acids. Arch Microbiol 164:406–413

    Article  CAS  Google Scholar 

  • Coates JD, Bhupathiraju VK, Achenbach LA, Mclnerney MJ, Lovley DR (2001) Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588

    Article  CAS  Google Scholar 

  • Cooper DC, Picardal F, Rivera J, Talbot C (2000) Zinc immobilization and magnetite formation via ferric oxide reduction by Shewanella putrefaciens 200. Environ Sci Technol 34:100–106

    Article  CAS  Google Scholar 

  • Cummings DE, Snoeyenbos-West OL, Newby DT, Niggemyer AM, Lovley DR, Achenbach LA, Rosenzweig RF (2003) Diversity of Geobacteraceae species inhabiting metal-polluted freshwater lake sediments ascertained by 16S rDNA analyses. Microb Ecol 46:257–269

    Article  CAS  Google Scholar 

  • Ding LJ, An XL, Li S, Zhang GL, Zhu YG (2014) Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ Sci Technol 48:10641–10647

    Article  CAS  Google Scholar 

  • Ding LJ, Su JQ, Xu HJ, Jia ZJ, Zhu YG (2015) Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. ISME J 9:721–734

    Article  CAS  Google Scholar 

  • Ding BJ, Li ZK, Qin YB (2017) Nitrogen loss from anaerobic ammonium oxidation coupled to Iron (III) reduction in a riparian zone. Environ Pollut 231:379–386

    Article  CAS  Google Scholar 

  • Dubinsky EA, Silver WL, Firestone MK (2010) Tropical forest soil microbial communities couple iron and carbon biogeochemistry. Ecology 91:2604–2612

    Article  Google Scholar 

  • Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JLM, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6:592–603

    Article  CAS  Google Scholar 

  • Haller L, Tonolla M, Zopfi J, Peduzzi R, Wildi W, Pote J (2011) Composition of bacterial and archaeal communities in freshwater sediments with different contamination levels (Lake Geneva, Switzerland). Water Res 45:1213–1228

    Article  CAS  Google Scholar 

  • Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258

    Article  CAS  Google Scholar 

  • Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579

    Article  CAS  Google Scholar 

  • Holmer M, Storkholm P (2001) Sulphate reduction and Sulphur cycling in lake sediments: a review. Freshw Biol 46:431–451

    Article  CAS  Google Scholar 

  • Holmes DE, Finneran KT, O'Neil RA, Lovley DR (2002) Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl Environ Microbiol 68:2300–2306

    Article  CAS  Google Scholar 

  • Holmes DE, O'Neil RA, Vrionis HA, N'Guessan LA, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP, Chavan MA, Johnson JP, Long PE, Lovley DR (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1:663–677

    Article  CAS  Google Scholar 

  • Ivanova EP, Sawabe T, Zhukova NV, Gorshkova NM, Nedashkovskaya OI, Hayashi K, Frolova GM, Sergeev AF, Pavel KG, Mikhailov VV, Nicolau DV (2003) Occurrence and diversity of mesophilic Shewanella strains isolated from the north-West Pacific Ocean. Syst Appl Microbiol 26:293–301

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Jensen MM, Thamdrup B, Rysgaard S, Holmer M, Fossing H (2003) Rates and regulation of microbial iron reduction in sediments of the Baltic-North Sea transition. Biogeochemistry 65:295–317

    Article  Google Scholar 

  • Karvinen A, Lehtinen L, Kankaala P (2015) Variable effects of iron (Fe (III)) additions on potential methane production in boreal lake littoral sediments. Wetlands 35:137–146

    Article  Google Scholar 

  • Kim SJ, Koh DC, Park SJ, Cha IT, Park JW, Na JH, Roh Y, Ko KS, Kim K, Rhee SK (2012) Molecular analysis of spatial variation of iron-reducing bacteria in riverine alluvial aquifers of the Mankyeong River. J Microbiol 50:207–217

    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 3:404

    Article  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 

  • Li L, Qu Z, Jia R, Wang B, Wang Y, Qu D (2017a) Excessive input of phosphorus significantly affects microbial Fe(III) reduction in flooded paddy soils by changing the abundances and community structures of Clostridium and Geobacteraceae. Sci Total Environ 607–608:982–991

    Article  Google Scholar 

  • Li P, Jiang Z, Wang YH, Deng Y, Van Nostrand JD, Yuan T, Liu H, Wei DZ, Zhou JZ (2017b) Analysis of the functional gene structure and metabolic potential of microbial community in high arsenic groundwater. Water Res 123:268–276

    Article  CAS  Google Scholar 

  • Li BB, Cheng YY, Fan YY, Liu DF, Fang CY, Wu C, Li WW, Yang ZC, Yu HQ (2018) Estimates of abundance and diversity of Shewanella genus in natural and engineered aqueous environments by newly designed primers. Sci Total Environ 637–638:926–933

    Article  Google Scholar 

  • Lin B (2006) Composition and functioning of iron-reducing communities in two contrasting environments, i.e., a landfill leachate-polluted aquifer and estuarine sediments. Ph.D. Thesis, Free University of Amsterdam, pp 1–165

  • Lin XJ, Kennedy D, Peacock A, McKinley J, Resch CT, Fredrickson J, Konopka A (2012) Distribution of microbial biomass and potential for anaerobic respiration in Hanford site 300 area subsurface sediment. Appl Environ Microbiol 78:759–767

    Article  CAS  Google Scholar 

  • Liu GF, Zhou JT, Chen CC, Wang J, Jin RF, Lv H (2013) Decolorization of azo dyes by Geobacter metallireducens. Appl Microbiol Biotechnol 97:7935–7942

    Article  CAS  Google Scholar 

  • Lovley DR (2013) Dissimilatory Fe (III)-and Mn (IV)-reducing prokaryotes. The prokaryotes. Springer, New York, p 1143

    Google Scholar 

  • Lovley DR, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286

    Article  CAS  Google Scholar 

  • Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru AE, Holmes DE (2011) Geobacter: the microbe electric's physiology ecology and practical applications. Adv Microb Physiol 59:1–100

  • Lu YH, Rosencrantz D, Liesack W, Conrad R (2006) Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ Microbiol 8:1351–1360

    Article  CAS  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nevin KP, Holmes DE, Woodard TL, Hinlein ES, Ostendorf DW, Lovley DR (2005) Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int J Syst Evol Microbiol 55:1667–1674

    Article  CAS  Google Scholar 

  • Peng QA, Shaaban M, Wu YP, Hu RG, Wang BY, Wang J (2016) The diversity of iron reducing bacteria communities in subtropical paddy soils of China. Appl Soil Ecol 101:20–27

    Article  Google Scholar 

  • Qian JZ, Wang LL, Zhan HB, Chen Z (2011) Urban land-use effects on groundwater phosphate distribution in a shallow aquifer, Nanfei River basin, China. Hydrogeol J 19:1431–1442

    Article  CAS  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 

  • Reyes C, Dellwig O, Dähnke K, Gehre M, Noriega-Ortega BE, Böttcher ME, Meister P, Friedrich MW (2016) Bacterial communities potentially involved in iron-cycling in Baltic Sea and North Sea sediments revealed by pyrosequencing. FEMS Microbiol Ecol 92:1–14

    Article  Google Scholar 

  • Röling FM (2014) The family Geobacteraceae. The prokaryotes. Springer, New York, pp 157–172

    Book  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Schumacher BA (2002) Methods for the determination of the total organic carbon (TOC) in soils and sediments. U.S. Environmental Protection Agency, Washington DC

    Google Scholar 

  • Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb Ecol 39:153–167

    Article  CAS  Google Scholar 

  • Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671

    Article  CAS  Google Scholar 

  • Stookey LL (1970) Ferrozine-a new spectrophotometric reagent for iron. Anal Chem 42:779–781

    Article  CAS  Google Scholar 

  • Stults JR, Snoeyenbos-West OL, Methe B, Lovley DR, Chandler DP (2001) Application of the 5′ fluorogenic exonuclease assay (TaqMan) for quantitative ribosomal DNA and rRNA analysis in sediments. Appl Environ Microbiol 67:2781–2789

    Article  CAS  Google Scholar 

  • Sun M, Xiao TF, Ning ZP, Xiao EZ, Sun WM (2015) Microbial community analysis in rice paddy soils irrigated by acid mine drainage contaminated water. Appl Microbiol Biotechnol 99:2911–2922

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  Google Scholar 

  • Thomsen U, Thamdrup B, Stahl DA, Canfield DE (2004) Pathways of organic carbon oxidation in a deep lacustrine sediment, Lake Michigan. Limnol Oceanogr 49:2046–2057

    Article  CAS  Google Scholar 

  • Wang J, Wu MY, Lu G, Si YB (2016) Biotransformation and biomethylation of arsenic by Shewanella oneidensis MR-1. Chemosphere 145:329–335

    Article  CAS  Google Scholar 

  • Woodhouse JN, Kinsela AS, Collins RN, Bowling LC, Honeyman GL, Holliday JK, Neilan BA (2016) Microbial communities reflect temporal changes in cyanobacterial composition in a shallow ephemeral freshwater lake. ISME J 10:1337–1351

    Article  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 

  • Zachara JM, Fredrickson JK, Smith SC, Gassman PL (2001) Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium. Geochim Cosmochim Acta 65:75–93

    Article  CAS  Google Scholar 

  • Zhang GY, He JZ, Liu F, Zhang LM (2014) Iron-manganese nodules harbor lower bacterial diversity and greater proportions of Proteobacteria compared to bulk soils in four locations spanning from north to South China. Geomicrobiol J 31:562–577

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank the National Natural Science Foundation of China (21477120, 21590812, 21607146 and 51878638), the Open Project of State Key Laboratory of Pollution Control and Resource Reuse, Nanjing University (PCRRF17024) and the Fundamental Research Funds for the Central Universities (WK2060190087) for the partial support to this work.

Author information

Author notes

  1. Yang-Yang Fan and Bing-Bing Li contributed equally to this work.

Authors and Affiliations

  1. School of Life Sciences, University of Science & Technology of China, Hefei, 230026, China

    Yang-Yang Fan, Bing-Bing Li & Zong-Chuang Yang

  2. CAS Key Laboratory of Urban Pollutant Conversion, Department of Chemistry, University of Science & Technology of China, Hefei, 230026, China

    Yang-Yang Fan, Bing-Bing Li, Yuan-Yuan Cheng, Dong-Feng Liu & Han-Qing Yu

Authors
  1. Yang-Yang Fan
    View author publications

    Search author on:PubMed Google Scholar

  2. Bing-Bing Li
    View author publications

    Search author on:PubMed Google Scholar

  3. Zong-Chuang Yang
    View author publications

    Search author on:PubMed Google Scholar

  4. Yuan-Yuan Cheng
    View author publications

    Search author on:PubMed Google Scholar

  5. Dong-Feng Liu
    View author publications

    Search author on:PubMed Google Scholar

  6. Han-Qing Yu
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Dong-Feng Liu.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(PDF 576 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, YY., Li, BB., Yang, ZC. et al. Abundance and diversity of iron reducing bacteria communities in the sediments of a heavily polluted freshwater lake. Appl Microbiol Biotechnol 102, 10791–10801 (2018). https://doi.org/10.1007/s00253-018-9443-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9443-1

Keywords