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Assessment of Microbial Communities Associated with Fermentative Assessment of microbial communities associated with fermentative–methanogenic biodegradation of aromatic hydrocarbons in groundwater contaminated with a biodiesel blend (B20) Débora Toledo Ramos, Márcio Luís Busi da Silva, Carlos Wolfgang Nossa, Pedro J. J. Alvarez & Henry Xavier Corseuil Biodegradation ISSN 0923-9820 Biodegradation DOI 10.1007/s10532-014-9691-4 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Biodegradation DOI 10.1007/s10532-014-9691-4 ORIGINAL PAPER Assessment of microbial communities associated with fermentative–methanogenic biodegradation of aromatic hydrocarbons in groundwater contaminated with a biodiesel blend (B20) De´bora Toledo Ramos • Ma´rcio Luı´s Busi da Silva • Carlos Wolfgang Nossa • Pedro J. J. Alvarez • Henry Xavier Corseuil Received: 5 December 2013 / Accepted: 9 April 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract A controlled field experiment was con- concomitantly with the increase in the relative abun- ducted to assess the potential for fermentative–meth- dance of Desulfitobacterium and Geobacter spp. (from anogenic biostimulation (by ammonium-acetate 5 to 52.7 % and 15.8 to 37.3 % of total Bacteria 16S injection) to enhance biodegradation of benzene, rRNA, respectively), which are known to anaerobi- toluene, ethylbenzene and xylenes (BTEX) as well cally degrade hydrocarbons. The accumulation of as polycyclic aromatic hydrocarbons (PAHs) in anaerobic metabolites acetate and hydrogen that could groundwater contaminated with biodiesel B20 (20:80 hinder the thermodynamic feasibility of BTEX and v/v soybean biodiesel and diesel). Changes in micro- PAH biotransformations under fermentative/methano- bial community structure were assessed by pyrose- genic conditions was apparently alleviated by the quencing 16S rRNA analyses. BTEX and PAH growing predominance of Methanosarcina. This sug- removal began 0.7 year following the release, gests the importance of microbial population shifts that enrich microorganisms capable of interacting syntrophically to enhance the feasibility of fermenta- D. T. Ramos (&) Á H. X. Corseuil tive–methanogenic bioremediation of biodiesel blend Department of Sanitary and Environmental Engineering, releases. Federal University of Santa Catarina, Floriano´polis, SC, Brazil e-mail: [email protected] Keywords Biodegradation Á Biodiesel Á BTEX Á H. X. Corseuil PAH Á Pyrosequencing Á Syntrophy e-mail: [email protected] M. L. B. da Silva Introduction EMBRAPA, BR 153 km 110, P.O. Box 21, Conco´rdia, SC 89700-000, Brazil e-mail: [email protected] The use of biodiesel blends as an alternative renewable transportation fuel is increasing worldwide to alleviate C. W. Nossa dependence on fossil fuels and to minimize atmo- Department of Ecology and Evolutionary Biology, Rice University, Houston, TX, USA spheric emissions and greenhouse effects. The e-mail: [email protected] increasing biodiesel demand can, however, increase the probability of groundwater contamination as result P. J. J. Alvarez of accidental and incidental spills during its produc- Department of Civil and Environmental Engineering, Rice University, Houston, TX, USA tion, transportation and storage. Although biodiesel is e-mail: [email protected] commonly referred to as a harmless and readily 123 Author's personal copy Biodegradation Table 1 Main reactions involved in biodiesel, BTEX and PAH degradation and DG°0 values (kJ mol-1) Reactions involved in linoleic acid (1, 2, 3 and 4), benzene (5, 6, 7 and 8) and naphthalene DG°0 reactiona (9, 10, 11 and 12) degradation (kJ mol-1) Linoleic acid (C18:2) - ? - ? (1) C18H31O2 ? H ? 16H2O ? 9CH3COO ? 9H ? 14H2 ?272.33 - ? (2) 9CH3COO ? 9H ? 18H2O? 36H2 ? 18CO2 ?854.26 (3) 50H2 ? 12,5CO2 ? 12,5CH4 ? 25H2O -1634.34 - ? (4) Sum (1) ? (2) ? (3): C18H31O2 ? H ? 9H2O ? 12,5CH4 ? 5,5CO2 -507.75 Benzene - ? (5) C6H6 ? 6H2O ? 3CH3COO ? 3H ? 3H2 ?70.73 - ? (6) 3CH3COO ? 3H ? 6H2O ? 12H2 ? 6CO2 ?284.754 (7) 15H2 ? 3,75CO2 ? 3,75CH4 ? 7,5H2O -490.30 (8) Sum (5) ? (6) ? (7): C6H6 ? 4,5 H2O ? 3.75CH4 ? 2.25CO2 -134.82 Naphthalene - ? (9) C10H8 ? 10H2O ? 5CH3COO ? 5H ? 4H2 ?101.12 - ? (10) 5CH3COO ? 5H ? 10H2O ? 10CO2 ? 20H2 ?474.59 (11) 24H2 ? 6CO2 ? 6CH4 ? 12H2O -784.48 (12) Sum (9) ? (10) ? (11): C10H8 ? 8H2O ? 6CH4 ? 4CO2 -291.75 DGf°(aq) values of linoleic acid and naphthalene were obtained in Lalman (2000) and Dolfing et al. (2009), respectively. All other compounds DGf° (aq and g (for H2)) values were obtained in Thauer et al. (1977) a Standard Gibbs energies were calculated under standard conditions (1 M solute concentration, pH = 7, T = 298 K and gas partial pressure of 1 atm) biodegradable biofuel (Zhang et al. 1998), it is usually methanogenic biotransformations are thermodynami- blended with petroleum diesel fuel that contains cally unfeasible (endergonic) (Table 1, reactions 1, 5 priority pollutants such as benzene, toluene, ethylben- and 9) without consumption of degradation byproducts zene and xylenes (BTEX) and polycyclic aromatic by commensal microorganisms. Long-chain fatty acids hydrocarbons (PAH). These hydrocarbons include (represented by linoleic acid) derived from biodiesel carcinogenic compounds (e.g., benzene and benzo[a]- esters hydrolysis can be further oxidized to acetate and pyrene) that are generally monitored to determine the hydrogen via b-oxidation (Sousa et al. 2009). Although need for corrective remedial action. this reaction is thermodynamically unfeasible (Table 1, The high biochemical oxygen demand exerted by reaction 1), it might proceed if syntrophic microorgan- indigenous microorganisms during biodiesel biodegra- isms consume metabolites that can impose thermody- dation rapidly drives impacted aquifers towards meth- namic constraints (reactions 2 and 3) thus making the anogenic conditions. This phenomenon is particularly overall reaction exergonic (reaction 4). Similarly, noticeable at the source zone region where higher fermentative/methanogenic BTEX and PAH biodegra- concentration of organic compounds stimulates the dation (represented by benzene and naphthalene, consumption of terminal electron acceptors. Under respectively) is plausible (reactions 8 and 12) when methanogenic conditions where the energetic yield is syntrophic microorganisms consume the metabolites close to the minimum needed for microbial sustenance (reactions 6, 7, 10 and 11). (&-20 kJ mol-1 required for ATP formation) (Schink We previously demonstrated that anaerobic biosti- 1997), bioremediation is usually accomplished by mulation by the addition of ammonium acetate into syntrophic microorganisms (Morris et al. 2013). Syn- B20 contaminated groundwater induced fermenta- trophic anaerobes can play a critical role in the tive–methanogenic conditions that enhanced BTEX biodegradation of long-chain fatty acids (Sousa et al. removal (Ramos et al. 2013). This enhancement in 2009), BTEX (Rakoczy et al. 2011)andPAH(Berdugo- BTEX anaerobic biodegradation was hypothesized to Clavijo et al. 2012), since initial fermentative/ occur due to the proliferation of putative hydrocarbon 123 Author's personal copy Biodegradation degraders thriving syntrophically with methanogenic and HP-5 capillary column). Detection limits were (in archaea. Nonetheless, the microbial community struc- parenthesis): naphthalene (7 lgL-1), methylnaphtha- ture was not characterized to identify potential lene (5 lgL-1), dimethylnaphthalene (7 lgL-1), ace- syntrophic associations. Therefore, in this work, naphthylene (8 lgL-1), acenaphthene (8 lgL-1), microbial 16S rRNA pyrosequencing analyses were fluorene (8 lgL-1), phenanthrene (9 lgL-1), conducted to assess temporal changes in microbial anthracene (9 lgL-1), fluorathene (10 lgL-1), pyr- community structure during anaerobic biostimulation ene (9 lgL-1), benzo[a]anthracene (9 lgL-1), chry- of groundwater contaminated with a biodiesel blend. sene (10 lgL-1), dibenzo[a,h]anthracene (12 lgL-1), Emphasis was placed on studying microbial popula- benzo[b]fluoranthene (12 lgL-1), benzo[k]fluo- tions putatively associated with aromatic hydrocarbon ranthene (31 lgL-1), benzo[a] pyrene (36 lgL-1), biodegradation. This information advances our current indeno[1,2,3-cd]pyrene (28 lgL-1) and benzo[g,h,i]- understanding of fermentative–methanogenic biopro- pyrene (11 lgL-1). cesses by identifying dominant microorganisms dur- Dissolved hydrogen analyses were conducted ing anaerobic bioremediation of B20 releases. 2.4 years following the B20 release using in situ passive samplers. These samplers were deployed for 5 days in groundwater, according to the methods Materials and methods developed by Spalding and Watson 2006 and Spalding and Watson 2008. Hydrogen was measured by a gas Controlled release field experiment chromatography (model UC-13 Construmaq equipped with a 30-ft long 9 1/8 in stainless-steel column A controlled
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