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A Novel Electrophototrophic Bacterium Rhodopseudomonas palustris Strain RP2, Exhibits Hydrocarbonoclastic Potential in Anaerobic Environments.

Venkidusamy K, Megharaj M - Front Microbiol (2016)

Bottom Line: Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, spore formation, anaerobic nitrate reduction, free living diazotrophy and the ability to degrade n-alkane components of petroleum hydrocarbons (PH) in anoxic, photic environments.The ability of strain RP2 to produce current (maximum current density 21 ± 3 mA/m(2); power density 720 ± 7 μW/m(2), 1000 Ω) using PH as a sole energy source was also examined using an initial concentration of 800 mg l(-1) of diesel range hydrocarbons (C9-C36) with a concomitant removal of 47.4 ± 2.7% hydrocarbons in MERS.Such observations reveal the importance of photoorganotrophic growth in the utilization of hydrocarbons from contaminated environments.

View Article: PubMed Central - PubMed

Affiliation: Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, SAAustralia; CRC for Contamination Assessment and Remediation of the Environment, Mawson Lakes, SAAustralia.

ABSTRACT
An electrophototrophic, hydrocarbonoclastic bacterium Rhodopseudomonas palustris stain RP2 was isolated from the anodic biofilms of hydrocarbon fed microbial electrochemical remediation systems (MERS). Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, spore formation, anaerobic nitrate reduction, free living diazotrophy and the ability to degrade n-alkane components of petroleum hydrocarbons (PH) in anoxic, photic environments. In acetate fed microbial electrochemical cells, a maximum current density of 305 ± 10 mA/m(2) (1000Ω) was generated (power density 131.65 ± 10 mW/m(2)) by strain RP2 with a coulombic efficiency of 46.7 ± 1.3%. Cyclic voltammetry studies showed that anaerobically grown cells of strain RP2 is electrochemically active and likely to transfer electrons extracellularly to solid electron acceptors through membrane bound compounds, however, aerobically grown cells lacked the electrochemical activity. The ability of strain RP2 to produce current (maximum current density 21 ± 3 mA/m(2); power density 720 ± 7 μW/m(2), 1000 Ω) using PH as a sole energy source was also examined using an initial concentration of 800 mg l(-1) of diesel range hydrocarbons (C9-C36) with a concomitant removal of 47.4 ± 2.7% hydrocarbons in MERS. Here, we also report the first study that shows an initial evidence for the existence of a hydrocarbonoclastic behavior in the strain RP2 when grown in different electron accepting and illuminated conditions (anaerobic and MERS degradation). Such observations reveal the importance of photoorganotrophic growth in the utilization of hydrocarbons from contaminated environments. Identification of such novel petrochemical hydrocarbon degrading electricigens, not only expands the knowledge on the range of bacteria known for the hydrocarbon bioremediation but also shows a biotechnological potential that goes well beyond its applications to MERS.

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Micrographs of spore formation in chemosynthetically grown cells of R. palustris strain RP2. (A) SEM micrograph. (B) TEM micrograph.
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Figure 1: Micrographs of spore formation in chemosynthetically grown cells of R. palustris strain RP2. (A) SEM micrograph. (B) TEM micrograph.

Mentions: The cells of strain RP2 have exceptionally flexible growth based on environmental signals such as photoorganotrophic, photolithotrophic, dark fermentative, and aerobic heterotrophic mechanisms. Optimum bacterial growth was observed at 25 to 30°C at a neutral pH, whilst no growth was detected above 40°C. Experiments to determine the growth factor requirements for the strain RP2 clearly shows the need for p-aminobenzoate, pyridoxine HCl, and folic acid (Supplementary Table S1). Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, anaerobic nitrate reduction, carbon dioxide fixation, free living diazotrophy, and the ability to degrade n-alkane components of PH under anoxic environments. Strain RP2 showed growth in minimal medium in the absence of both nitrogen and carbon sources under anoxic, photosynthetic conditions. Nitrogen fixation trait was confirmed by the detection of a nifH gene required for nitrogen fixation in the strain. The strain RP2 differed from a previously reported exoelectrogenic strain of R. palustris DX1 (Xing et al., 2008) with respect to its ability of photoassimilating a range of substrates including gluconate, aspartate, glycerol, and amino-ethanol. However, the strain RP2 was unable to utilize some compounds such as sebacic acid, threonine, L-ornithine, and L-proline. The ability to utilize sodium benzoate distinguishes the strain from other species of purple sulfur bacteria. The strain RP2 can assimilate acetate photosynthetically with nitrate, sulfate, and iron as terminal electron acceptors (Supplementary Figure S3). We cultured RP2 cells under two different environmental conditions: anoxic photoheterotrophic and anoxic chemoheterotrophic with crystalline Fe(III) oxide as a terminal electron acceptor to investigate the dissimilatory metal oxide reduction trait. Fe(III) oxide reduction was monitored by color change and hydroxylamine Fe(II)extraction assay. Fe(III) oxide reduction of 69.5% ± 0.41% was observed only in anoxic photoheterotrophic environments (Venkidusamy et al., 2015) whereas chemosynthetic grown cells showed no reduction. During this process, peculiar extracellular electrically conductive nanofilamentous structures were observed in the phototrophic growth conditions as stated previously (Venkidusamy et al., 2015). When colonies are incubated for longer incubations (for a period of 4-5 weeks) under anoxic chemosynthetic conditions, they develop a complex morphology such as spore formation with a well-defined outer layer (Figure 1).


A Novel Electrophototrophic Bacterium Rhodopseudomonas palustris Strain RP2, Exhibits Hydrocarbonoclastic Potential in Anaerobic Environments.

Venkidusamy K, Megharaj M - Front Microbiol (2016)

Micrographs of spore formation in chemosynthetically grown cells of R. palustris strain RP2. (A) SEM micrograph. (B) TEM micrograph.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4940424&req=5

Figure 1: Micrographs of spore formation in chemosynthetically grown cells of R. palustris strain RP2. (A) SEM micrograph. (B) TEM micrograph.
Mentions: The cells of strain RP2 have exceptionally flexible growth based on environmental signals such as photoorganotrophic, photolithotrophic, dark fermentative, and aerobic heterotrophic mechanisms. Optimum bacterial growth was observed at 25 to 30°C at a neutral pH, whilst no growth was detected above 40°C. Experiments to determine the growth factor requirements for the strain RP2 clearly shows the need for p-aminobenzoate, pyridoxine HCl, and folic acid (Supplementary Table S1). Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, anaerobic nitrate reduction, carbon dioxide fixation, free living diazotrophy, and the ability to degrade n-alkane components of PH under anoxic environments. Strain RP2 showed growth in minimal medium in the absence of both nitrogen and carbon sources under anoxic, photosynthetic conditions. Nitrogen fixation trait was confirmed by the detection of a nifH gene required for nitrogen fixation in the strain. The strain RP2 differed from a previously reported exoelectrogenic strain of R. palustris DX1 (Xing et al., 2008) with respect to its ability of photoassimilating a range of substrates including gluconate, aspartate, glycerol, and amino-ethanol. However, the strain RP2 was unable to utilize some compounds such as sebacic acid, threonine, L-ornithine, and L-proline. The ability to utilize sodium benzoate distinguishes the strain from other species of purple sulfur bacteria. The strain RP2 can assimilate acetate photosynthetically with nitrate, sulfate, and iron as terminal electron acceptors (Supplementary Figure S3). We cultured RP2 cells under two different environmental conditions: anoxic photoheterotrophic and anoxic chemoheterotrophic with crystalline Fe(III) oxide as a terminal electron acceptor to investigate the dissimilatory metal oxide reduction trait. Fe(III) oxide reduction was monitored by color change and hydroxylamine Fe(II)extraction assay. Fe(III) oxide reduction of 69.5% ± 0.41% was observed only in anoxic photoheterotrophic environments (Venkidusamy et al., 2015) whereas chemosynthetic grown cells showed no reduction. During this process, peculiar extracellular electrically conductive nanofilamentous structures were observed in the phototrophic growth conditions as stated previously (Venkidusamy et al., 2015). When colonies are incubated for longer incubations (for a period of 4-5 weeks) under anoxic chemosynthetic conditions, they develop a complex morphology such as spore formation with a well-defined outer layer (Figure 1).

Bottom Line: Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, spore formation, anaerobic nitrate reduction, free living diazotrophy and the ability to degrade n-alkane components of petroleum hydrocarbons (PH) in anoxic, photic environments.The ability of strain RP2 to produce current (maximum current density 21 ± 3 mA/m(2); power density 720 ± 7 μW/m(2), 1000 Ω) using PH as a sole energy source was also examined using an initial concentration of 800 mg l(-1) of diesel range hydrocarbons (C9-C36) with a concomitant removal of 47.4 ± 2.7% hydrocarbons in MERS.Such observations reveal the importance of photoorganotrophic growth in the utilization of hydrocarbons from contaminated environments.

View Article: PubMed Central - PubMed

Affiliation: Centre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, SAAustralia; CRC for Contamination Assessment and Remediation of the Environment, Mawson Lakes, SAAustralia.

ABSTRACT
An electrophototrophic, hydrocarbonoclastic bacterium Rhodopseudomonas palustris stain RP2 was isolated from the anodic biofilms of hydrocarbon fed microbial electrochemical remediation systems (MERS). Salient properties of the strain RP2 were direct electrode respiration, dissimilatory metal oxide reduction, spore formation, anaerobic nitrate reduction, free living diazotrophy and the ability to degrade n-alkane components of petroleum hydrocarbons (PH) in anoxic, photic environments. In acetate fed microbial electrochemical cells, a maximum current density of 305 ± 10 mA/m(2) (1000Ω) was generated (power density 131.65 ± 10 mW/m(2)) by strain RP2 with a coulombic efficiency of 46.7 ± 1.3%. Cyclic voltammetry studies showed that anaerobically grown cells of strain RP2 is electrochemically active and likely to transfer electrons extracellularly to solid electron acceptors through membrane bound compounds, however, aerobically grown cells lacked the electrochemical activity. The ability of strain RP2 to produce current (maximum current density 21 ± 3 mA/m(2); power density 720 ± 7 μW/m(2), 1000 Ω) using PH as a sole energy source was also examined using an initial concentration of 800 mg l(-1) of diesel range hydrocarbons (C9-C36) with a concomitant removal of 47.4 ± 2.7% hydrocarbons in MERS. Here, we also report the first study that shows an initial evidence for the existence of a hydrocarbonoclastic behavior in the strain RP2 when grown in different electron accepting and illuminated conditions (anaerobic and MERS degradation). Such observations reveal the importance of photoorganotrophic growth in the utilization of hydrocarbons from contaminated environments. Identification of such novel petrochemical hydrocarbon degrading electricigens, not only expands the knowledge on the range of bacteria known for the hydrocarbon bioremediation but also shows a biotechnological potential that goes well beyond its applications to MERS.

No MeSH data available.


Related in: MedlinePlus