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Frontiers of Environmental Science & Engineering

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Front. Environ. Sci. Eng.    2015, Vol. 9 Issue (3) : 453-464    https://doi.org/10.1007/s11783-014-0721-6
RESEARCH ARTICLE
Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing
Mary Beth LEIGH1,2,*(),Wei-Min WU3,*(),Erick CARDENAS1,Ondrej UHLIK4,Sue CARROLL5,Terry GENTRY5,7,Terence L. MARSH1,Jizhong ZHOU5,6,Philip JARDINE5,Craig S. CRIDDLE3,James M. TIEDJE1
1. Center for Microbial Ecology, Michigan State University, East Lansing, MI 48824, USA
2. Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775, USA
3. Department of Civil and Environmental Engineering, Center for Sustainable Development & Global Competitiveness, Codiga Resource Recovery Center, Stanford University, Stanford, CA 94305-4020, USA
4. Department of Biochemistry and Microbiology, Institute of Chemical Technology Prague, Technicka 3, 166 28 Prague, Czech Republic
5. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA
6. Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73019, USA
7. Department of Crop and Soil Sciences, Texas A&M University, College Station, TX 77843, USA
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Abstract

Stable isotope probing (SIP) was used to identify microbes stimulated by ethanol addition in microcosms containing two sediments collected from the bioremediation test zone at the US Department of Energy Oak Ridge site, TN, USA. One sample was highly bioreduced with ethanol while another was less reduced. Microcosms with the respective sediments were amended with 13C labeled ethanol and incubated for 7 days for SIP. Ethanol was rapidly converted to acetate within 24 h accompanied with the reduction of nitrate and sulfate. The accumulation of acetate persisted beyond the 7 d period. Aqueous U did not decline in the microcosm with the reduced sediment due to desorption of U but continuously declined in the less reduced sample. Microbial growth and concomitant 13C-DNA production was detected when ethanol was exhausted and abundant acetate had accumulated in both microcosms. This coincided with U(VI) reduction in the less reduced sample. 13C originating from ethanol was ultimately utilized for growth, either directly or indirectly, by the dominant microbial community members within 7 days of incubation. The microbial community was comprised predominantly of known denitrifiers, sulfate-reducing bacteria and iron (III) reducing bacteria including Desulfovibrio, Sphingomonas, Ferribacterium, Rhodanobacter, Geothrix, Thiobacillus and others, including the known U(VI)-reducing bacteria Acidovorax, Anaeromyxobacter, Desulfovibrio, Geobacter and Desulfosporosinus. The findings suggest that ethanol biostimulates the U(VI)-reducing microbial community by first serving as an electron donor for nitrate, sulfate, iron (III) and U(VI) reduction, and acetate which then functions as electron donor for U(VI) reduction and carbon source for microbial growth.
Keywords Stable isotope probing (SIP)      ethanol      acetate      uranium reduction      sediment      bioremediation     
Corresponding Author(s): Mary Beth LEIGH,Wei-Min WU   
Online First Date: 19 June 2014    Issue Date: 30 April 2015
 Cite this article:   
Mary Beth LEIGH,Wei-Min WU,Erick CARDENAS, et al. Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing[J]. Front. Environ. Sci. Eng., 2015, 9(3): 453-464.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-014-0721-6
https://academic.hep.com.cn/fese/EN/Y2015/V9/I3/453
microcosm FW104 FW026
groundwater
??pH 5.88 5.86
?? H C O 3 - , mmol·L-1 1.3 1.1
?? S O 4 2 - , mmol·L-1 1.38 1.95
?? S 2 - , mmol·L-1 0.18 0.023
??NO3-, mmol·L-1 0 0.001
??Cl-, mmol·L-1 2.57 2.57
??U, μg·L-1 129 132
??Fe, mmol·L-1 0.028 0.025
??Na+, mmol·L-1 1.71 1.90
??K+, mmol·L-1 0.59 0.63
??Ca2+, mmol·L-1 0.62 0.64
??Mg2+, mmol·L-1 0.33 0.36
??Mn2+, mmol·L-1 0.063 0.064
??Be, mmol·L-1 0.014 0.014
??COD, mg·L-1 146 9
sediment
??U content, m·kg-1 6.0 1.20
??U(VI) in total U, % 60 <10
??Fe content, g·kg-1 199 47
??Fe(II) in total Fe, % 53% 10%
??Sulfide content, mg·kg-1 23 0
Tab.1  Chemical composition of groundwater and sediment samples used for microcosm test
well sample type MPN
denitrifiers SRB FeRB
groundwater (cells·mL-1)
FW104 (injection) groundwater 9.4 × 105 5.4 × 106 1.4× 104
FW026 (extraction) groundwater 2.8 × 105 5.5 × 105 5.1× 105
sediment (cells·g-1 dry weight)
FW104 (injection) sediment 7.2 × 108 1.53 × 108 9.4 × 107
FW026 (extraction) sediment 1.1 × 107 1.1 × 106 1.9 × 106
Tab.2  Most probable numbers (MPN) of denitrifiers, sulfate reducing bacteria (SRB) and iron (III) reducing bacteria (FeRB) in groundwater and sediment samples used for microcosm test.
organism relative abundance /%a electron acceptor electron donor T-RF length (bp) T-RF label on Fig.3
FW104 FW026 Fe(III) Nitrate Sulfate U(VI) Ethanol Acetate
Acidobacteria
??Geothrix 11.0 15.5 + + - ? - + 96, 375 B, E
Chloroflexi
??Anaerolinea 1.9 7.7 - - - ? - - 213 C
Firmicutes
??Desulfosporosinus 1.3 0.0 + -* + + + + 386 nd
Gemmatimoadetes
??Gemmatimonas 1.3 0.0 - - - - - + 360 D
Proteobacteria
??Acidovorax 1.9 0.7 - + - ?* + + 204 C
??Anaeromyxobacter 0.6 0.0 + + - + ? + 94, 224 B
??Desulfovibrio 6.5 5.6 + + + + + - 95 B
??Duganella 9.0 0.7 ? - ? ? + + 67 A
??Ferribacterium 11 14.1 + + - ? – + 67, 207 A, C
??Geobacter 2.6 0.7 + + - + + + 95 B
??Thiobacillus 4.5 4.9 -* + - ? -* - 67, 451,570 A, F, G
??Rhodoferax 0.0 3.5 + + - - - + 206 C
??Rhodanobacter 6.5 0.0 ? - - ? - ? 209 C
??Sterolibacterium 0.0 1.4 ? + ? ? - - 67 A
??Sphingomonas 5.2 0.7 ? + ? ? ? -* 96 B
Tab.3  Dominant microorganisms detected in the sediment samples and predicated terminal restriction fragments (T-RF) length.
Fig.1  T-RFLP profiles of total community DNA, heavy background control DNA (representing contamination) and heavy DNA following 7 d incubation with 13C-ethanol for each microcosm.

Refer to Table 3 for T-RF sizes. T-RFs matched to clone sequences based on in silico digestions are labeled as follows A. Duganella*, Ferribacterium, Sterolibacterium, Thiobacillus; B. Desulfovibrio**, Sphingomonas**, Geobacter, Geothrix, Anaeromyxobacter; C. Ferribacterium**, Rhodanobacter**, Rhodoferax*, Anaerolinea**, Acidovorax* ; D. Gemmatimonas, E. Geothrix**, F. Thiobacillus*, G. Thiobacillus.

*=Sequence associate with T-RF abundant in clone libraries. ** =Abundant in clone libraries (>5% of clones, Table 3).

Fig.2  Concentrations of (a) ethanol; (b) acetate ; (c) nitrate; (d) sulfate; (e) sulfide; and (f) U(VI) in microcosms during the SIP incubation period.
Fig.3  Quantitation of 16S rRNA genes in density gradient fractions at initiation of experiment (0 h) and following 168 h incubation with 13C-ethanol. Y axis shows abundance of 16S rRNA gene copies as a ratio of the maximum copies detected in each gradient.
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