Identification of Electrode Respiring, Hydrocarbonoclastic Bacterial Strain Stenotrophomonas maltophilia MK2 Highlights the Untapped Potential for Environmental Bioremediation

Abstract

Electrode respiring bacteria (ERB) possess a great potential for many biotechnological applications such as microbial electrochemical remediation systems (MERS) because of their exoelectrogenic capabilities to degrade xenobiotic pollutants. Very few ERB have been isolated from MERS, those exhibited a bioremediation potential toward organic contaminants. Here we report once such bacterial strain, Stenotrophomonas maltophilia MK2, a facultative anaerobic bacterium isolated from a hydrocarbon fed MERS, showed a potent hydrocarbonoclastic behavior under aerobic and anaerobic environments. Distinct properties of the strain MK2 were anaerobic fermentation of the amino acids, electrode respiration, anaerobic nitrate reduction and the ability to metabolize n-alkane components (C8–C36) of petroleum hydrocarbons (PH) including the biomarkers, pristine and phytane. The characteristic of diazoic dye decolorization was used as a criterion for pre-screening the possible electrochemically active microbial candidates. Bioelectricity generation with concomitant dye decolorization in MERS showed that the strain is electrochemically active. In acetate fed microbial fuel cells (MFCs), maximum current density of 273 ± 8 mA/m2 (1000 Ω) was produced (power density 113 ± 7 mW/m2) by strain MK2 with a coulombic efficiency of 34.8%. Further, the presence of possible alkane hydroxylase genes (alkB and rubA) in the strain MK2 indicated that the genes involved in hydrocarbon degradation are of diverse origin. Such observations demonstrated the potential of facultative hydrocarbon degradation in contaminated environments. Identification of such a novel petrochemical hydrocarbon degrading ERB is likely to offer a new route to the sustainable bioremedial process of source zone contamination with simultaneous energy generation through MERS.

Petrophilic, Fe(III) Reducing Exoelectrogen Citrobacter sp. KVM11, Isolated From Hydrocarbon Fed Microbial Electrochemical Remediation Systems

“…In our laboratory, hydrocarbon fed MERS have been successfully demonstrated for the enhanced removal of PH contaminants ( Venkidusamy et al, 2016 ). The subsequent isolation and characterization of single bacterial species from the exoelectrogenic biofilms of PH fed MERS suggests that isolated bacterial strains gained an advantage of extracellular electrode respiration ( Venkidusamy et al, 2015 ; Venkidusamy and Megharaj, 2016a ) and Fe(III) reduction ( Venkidusamy and Megharaj, 2016b ) as reported earlier. In this study, we report one such Fe(III) reducing bacterial strain phylogenetically related to Citrobacter genus and designated as Citrobacter sp.…”

“…These systems offer a unique platform to study the electro-microbial process involved in bioremediation of oil pollutants ( Venkidusamy et al, 2016 ) and heavy metals ( Qiu et al, 2017 ; Wang et al, 2017 ), etc., The electroactive biofilms are those that have the capabilities of extracellular electron flow (EET) to degrade substrates that range from easily degradable natural organic compounds to xenobiotic compounds such as petroleum hydrocarbon (PH) contaminants ( Venkidusamy et al, 2016 ; Zhou et al, 2016 ). Such biofilms can be formed by a single bacterial species (pure strain) ( Venkidusamy and Megharaj, 2016a , b ) or by multiple bacterial species (mixed culture) ( Morris et al, 2009 ). The dominant view, until recently is that multiple bacterial species are better suited for its commercial applications ( Chae et al, 2009 ), while the single bacterial species are selected to study their physiology and electrochemical performance ( Xing et al, 2008 ; Zhi et al, 2014 ; Venkidusamy and Megharaj, 2016a , b ; Qiu et al, 2017 ).…”

“…Such biofilms can be formed by a single bacterial species (pure strain) ( Venkidusamy and Megharaj, 2016a , b ) or by multiple bacterial species (mixed culture) ( Morris et al, 2009 ). The dominant view, until recently is that multiple bacterial species are better suited for its commercial applications ( Chae et al, 2009 ), while the single bacterial species are selected to study their physiology and electrochemical performance ( Xing et al, 2008 ; Zhi et al, 2014 ; Venkidusamy and Megharaj, 2016a , b ; Qiu et al, 2017 ).…”

“…( Badalamenti et al, 2013 ) Clostridium butyricum ( Park et al, 2001 ) etc., which can transfer electrons to solid phase electron acceptors with co-degradation of recalcitrant contaminants ( Kunapuli et al, 2010 ). For instance, Rhodopseudomonas palustris strain RP2, a dissimilatory Fe(III) reducer isolated from PH fed MERS has been shown to produce a maximum current density of 21 ± 3 mA/m 2 ; with simultaneous removal of 47 ± 2.7% in MERS within 30 days ( Venkidusamy and Megharaj, 2016b ). It is important to note that the microbial community composition is divergent in MERS ( Morris et al, 2009 ; Venkidusamy et al, 2016 ) fed with contaminants such as petrochemicals and the physiology of such microbial populations remains to be explored.…”

Community dynamics and functional characteristics of naphthalene‐degrading populations in contaminated surface sediments and hypoxic/anoxic groundwater

“…Stenotrophomonas spp. are known to be facultatively anaerobic nitrate‐reducers (Ryan et al ., ) and are frequently prominent members of anode‐respiring communities in hydrocarbon degrading microbial fuel cells (Venkidusamy et al ., ; Venkidusamy and Megharaj, ) and in electrochemically‐stimulated remediation of hydrocarbon contaminated groundwater (Morris et al ., ) and soil (Lu et al ., ). The mechanism for electron shuttling to solid surfaces in Stenotrophomonas is not yet understood, but the capacity of Stenotrophomonas to reduce gold particles is indicative of a capacity for diverse redox coupling (Nangia et al ., ).…”