Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species

Continental subsurface environments can present significant energetic challenges to the resident microorganisms. While these environments are geologically diverse, potentially allowing energy harvesting by microorganisms that catalyze redox reactions, many of the abundant electron donors and accepto...

Full description

Bibliographic Details
Main Authors: Yamini eJangir, Sarah eFrench, Lily Melinda Momper, Duane P. Moser, Jan P. Amend, Mohamed Y. El-Naggar
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00756/full
_version_ 1818217449296756736
author Yamini eJangir
Sarah eFrench
Lily Melinda Momper
Duane P. Moser
Jan P. Amend
Jan P. Amend
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
author_facet Yamini eJangir
Sarah eFrench
Lily Melinda Momper
Duane P. Moser
Jan P. Amend
Jan P. Amend
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
author_sort Yamini eJangir
collection DOAJ
description Continental subsurface environments can present significant energetic challenges to the resident microorganisms. While these environments are geologically diverse, potentially allowing energy harvesting by microorganisms that catalyze redox reactions, many of the abundant electron donors and acceptors are insoluble and therefore not directly bioavailable. Extracellular electron transfer (EET) is a metabolic strategy that microorganisms can deploy to meet the challenges of interacting with redox-active surfaces. Though mechanistically characterized in a few metal-reducing bacteria, the role, extent, and diversity of EET in subsurface ecosystems remains unclear. Since this process can be mimicked on electrode surfaces, it opens the door to electrochemical techniques to enrich for and quantify the activities of environmental microorganisms in situ. Here, we report the electrochemical enrichment of microorganisms from a deep fractured-rock aquifer in Death Valley, California, USA. In experiments performed in mesocosms containing a synthetic medium based on aquifer chemistry, four working electrodes were poised at different redox potentials (272, 373, 472, 572 mV vs. SHE) to serve as electron acceptors, resulting in anodic currents coupled to the oxidation of acetate during enrichment. The anodes were dominated by Betaproteobacteria from the families Comamonadaceae and Rhodocyclaceae. A representative of each dominant family was subsequently isolated from electrode-associated biomass. The EET abilities of the isolated Delftia strain (designated WE1-13) and Azonexus strain (designated WE2-4) were confirmed in electrochemical reactors using working electrodes poised at 522 mV vs. SHE. The rise in anodic current upon inoculation was correlated with a modest increase in total protein content. Both genera have been previously observed in mixed communities of microbial fuel cell enrichments, but this is the first direct measurement of their electrochemical activity. While alternate metabolisms (e.g. nitrate reduction) by these organisms were previously known, our observations suggest that additional ‘hidden’ interactions with external electron acceptors are also possible. Electrochemical approaches are well positioned to dissect such extracellular interactions that may be prevalent in the subsurface.
first_indexed 2024-12-12T07:08:03Z
format Article
id doaj.art-aa192e217e074a549f2622803e9a93ed
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-12T07:08:03Z
publishDate 2016-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-aa192e217e074a549f2622803e9a93ed2022-12-22T00:33:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-05-01710.3389/fmicb.2016.00756198915Isolation and characterization of electrochemically active subsurface Delftia and Azonexus speciesYamini eJangir0Sarah eFrench1Lily Melinda Momper2Duane P. Moser3Jan P. Amend4Jan P. Amend5Mohamed Y. El-Naggar6Mohamed Y. El-Naggar7Mohamed Y. El-Naggar8University of Southern CaliforniaUniversity of Southern CaliforniaUniversity of Southern CaliforniaDesert Research InstituteUniversity of Southern CaliforniaUniversity of Southern CaliforniaUniversity of Southern CaliforniaUniversity of Southern CaliforniaUniversity of Southern CaliforniaContinental subsurface environments can present significant energetic challenges to the resident microorganisms. While these environments are geologically diverse, potentially allowing energy harvesting by microorganisms that catalyze redox reactions, many of the abundant electron donors and acceptors are insoluble and therefore not directly bioavailable. Extracellular electron transfer (EET) is a metabolic strategy that microorganisms can deploy to meet the challenges of interacting with redox-active surfaces. Though mechanistically characterized in a few metal-reducing bacteria, the role, extent, and diversity of EET in subsurface ecosystems remains unclear. Since this process can be mimicked on electrode surfaces, it opens the door to electrochemical techniques to enrich for and quantify the activities of environmental microorganisms in situ. Here, we report the electrochemical enrichment of microorganisms from a deep fractured-rock aquifer in Death Valley, California, USA. In experiments performed in mesocosms containing a synthetic medium based on aquifer chemistry, four working electrodes were poised at different redox potentials (272, 373, 472, 572 mV vs. SHE) to serve as electron acceptors, resulting in anodic currents coupled to the oxidation of acetate during enrichment. The anodes were dominated by Betaproteobacteria from the families Comamonadaceae and Rhodocyclaceae. A representative of each dominant family was subsequently isolated from electrode-associated biomass. The EET abilities of the isolated Delftia strain (designated WE1-13) and Azonexus strain (designated WE2-4) were confirmed in electrochemical reactors using working electrodes poised at 522 mV vs. SHE. The rise in anodic current upon inoculation was correlated with a modest increase in total protein content. Both genera have been previously observed in mixed communities of microbial fuel cell enrichments, but this is the first direct measurement of their electrochemical activity. While alternate metabolisms (e.g. nitrate reduction) by these organisms were previously known, our observations suggest that additional ‘hidden’ interactions with external electron acceptors are also possible. Electrochemical approaches are well positioned to dissect such extracellular interactions that may be prevalent in the subsurface.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00756/fullDelftiasubsurface microbiologybioelectrochemistryelectromicrobiologyAzonexus
spellingShingle Yamini eJangir
Sarah eFrench
Lily Melinda Momper
Duane P. Moser
Jan P. Amend
Jan P. Amend
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
Mohamed Y. El-Naggar
Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
Frontiers in Microbiology
Delftia
subsurface microbiology
bioelectrochemistry
electromicrobiology
Azonexus
title Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
title_full Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
title_fullStr Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
title_full_unstemmed Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
title_short Isolation and characterization of electrochemically active subsurface Delftia and Azonexus species
title_sort isolation and characterization of electrochemically active subsurface delftia and azonexus species
topic Delftia
subsurface microbiology
bioelectrochemistry
electromicrobiology
Azonexus
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00756/full
work_keys_str_mv AT yaminiejangir isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT sarahefrench isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT lilymelindamomper isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT duanepmoser isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT janpamend isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT janpamend isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT mohamedyelnaggar isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT mohamedyelnaggar isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies
AT mohamedyelnaggar isolationandcharacterizationofelectrochemicallyactivesubsurfacedelftiaandazonexusspecies