Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange

Pravin Malla Shrestha, Amelia-Elena Rotaru, Muktak Aklujkar, Fanghua Liu, Minita Shrestha, Zarath M Summers, Nikhil Malvankar, Dan Carlo Flores, Derek R Lovley

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

Direct interspecies electron transfer (DIET) through biological electrical connections is an alternative to interspecies H2 transfer as a mechanism for electron exchange in syntrophic cultures. However, it has not previously been determined whether electrons received via DIET yield energy to support cell growth. In order to investigate this, co-cultures of Geobacter metallireducens, which can transfer electrons to wild-type G. sulfurreducens via DIET, were established with a citrate synthase-deficient G. sulfurreducens strain that can receive electrons for respiration through DIET only. In a medium with ethanol as the electron donor and fumarate as the electron acceptor, co-cultures with the citrate synthase-deficient G. sulfurreducens strain metabolized ethanol as fast as co-cultures with wild-type, but the acetate that G. metallireducens generated from ethanol oxidation accumulated. The lack of acetate metabolism resulted in less fumarate reduction and lower cell abundance of G. sulfurreducens. RNAseq analysis of transcript abundance was consistent with a lack of acetate metabolism in G. sulfurreducens and revealed gene expression levels for the uptake hydrogenase, formate dehydrogenase, the pilus-associated c-type cytochrome OmcS and pili consistent with electron transfer via DIET. These results suggest that electrons transferred via DIET can serve as the sole energy source to support anaerobic respiration.
OriginalsprogEngelsk
TidsskriftEnvironmental Microbiology Reports
Vol/bind5
Udgave nummer6
Sider (fra-til)904-910
ISSN1758-2229
DOI
StatusUdgivet - 2013

Fingeraftryk

energy transfer
electron transfer
Electrons
electron
electrons
Growth
energy
coculture
citrate (si)-synthase
fimbriae
acetates
ethanol
Coculture Techniques
Geobacter metallireducens
Citrate (si)-Synthase
acetate
Ethanol
metabolism
anaerobiosis
cytochromes

Citer dette

Shrestha, Pravin Malla ; Rotaru, Amelia-Elena ; Aklujkar, Muktak ; Liu, Fanghua ; Shrestha, Minita ; Summers, Zarath M ; Malvankar, Nikhil ; Flores, Dan Carlo ; Lovley, Derek R. / Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. I: Environmental Microbiology Reports. 2013 ; Bind 5, Nr. 6. s. 904-910.
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title = "Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange",
abstract = "Direct interspecies electron transfer (DIET) through biological electrical connections is an alternative to interspecies H2 transfer as a mechanism for electron exchange in syntrophic cultures. However, it has not previously been determined whether electrons received via DIET yield energy to support cell growth. In order to investigate this, co-cultures of Geobacter metallireducens, which can transfer electrons to wild-type G. sulfurreducens via DIET, were established with a citrate synthase-deficient G. sulfurreducens strain that can receive electrons for respiration through DIET only. In a medium with ethanol as the electron donor and fumarate as the electron acceptor, co-cultures with the citrate synthase-deficient G. sulfurreducens strain metabolized ethanol as fast as co-cultures with wild-type, but the acetate that G. metallireducens generated from ethanol oxidation accumulated. The lack of acetate metabolism resulted in less fumarate reduction and lower cell abundance of G. sulfurreducens. RNAseq analysis of transcript abundance was consistent with a lack of acetate metabolism in G. sulfurreducens and revealed gene expression levels for the uptake hydrogenase, formate dehydrogenase, the pilus-associated c-type cytochrome OmcS and pili consistent with electron transfer via DIET. These results suggest that electrons transferred via DIET can serve as the sole energy source to support anaerobic respiration.",
author = "Shrestha, {Pravin Malla} and Amelia-Elena Rotaru and Muktak Aklujkar and Fanghua Liu and Minita Shrestha and Summers, {Zarath M} and Nikhil Malvankar and Flores, {Dan Carlo} and Lovley, {Derek R}",
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year = "2013",
doi = "10.1111/1758-2229.12093",
language = "English",
volume = "5",
pages = "904--910",
journal = "Environmental Microbiology Reports",
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Shrestha, PM, Rotaru, A-E, Aklujkar, M, Liu, F, Shrestha, M, Summers, ZM, Malvankar, N, Flores, DC & Lovley, DR 2013, 'Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange', Environmental Microbiology Reports, bind 5, nr. 6, s. 904-910. https://doi.org/10.1111/1758-2229.12093

Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. / Shrestha, Pravin Malla; Rotaru, Amelia-Elena; Aklujkar, Muktak; Liu, Fanghua; Shrestha, Minita; Summers, Zarath M; Malvankar, Nikhil; Flores, Dan Carlo; Lovley, Derek R.

I: Environmental Microbiology Reports, Bind 5, Nr. 6, 2013, s. 904-910.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange

AU - Shrestha, Pravin Malla

AU - Rotaru, Amelia-Elena

AU - Aklujkar, Muktak

AU - Liu, Fanghua

AU - Shrestha, Minita

AU - Summers, Zarath M

AU - Malvankar, Nikhil

AU - Flores, Dan Carlo

AU - Lovley, Derek R

N1 - © 2013 John Wiley & Sons Ltd and Society for Applied Microbiology.

PY - 2013

Y1 - 2013

N2 - Direct interspecies electron transfer (DIET) through biological electrical connections is an alternative to interspecies H2 transfer as a mechanism for electron exchange in syntrophic cultures. However, it has not previously been determined whether electrons received via DIET yield energy to support cell growth. In order to investigate this, co-cultures of Geobacter metallireducens, which can transfer electrons to wild-type G. sulfurreducens via DIET, were established with a citrate synthase-deficient G. sulfurreducens strain that can receive electrons for respiration through DIET only. In a medium with ethanol as the electron donor and fumarate as the electron acceptor, co-cultures with the citrate synthase-deficient G. sulfurreducens strain metabolized ethanol as fast as co-cultures with wild-type, but the acetate that G. metallireducens generated from ethanol oxidation accumulated. The lack of acetate metabolism resulted in less fumarate reduction and lower cell abundance of G. sulfurreducens. RNAseq analysis of transcript abundance was consistent with a lack of acetate metabolism in G. sulfurreducens and revealed gene expression levels for the uptake hydrogenase, formate dehydrogenase, the pilus-associated c-type cytochrome OmcS and pili consistent with electron transfer via DIET. These results suggest that electrons transferred via DIET can serve as the sole energy source to support anaerobic respiration.

AB - Direct interspecies electron transfer (DIET) through biological electrical connections is an alternative to interspecies H2 transfer as a mechanism for electron exchange in syntrophic cultures. However, it has not previously been determined whether electrons received via DIET yield energy to support cell growth. In order to investigate this, co-cultures of Geobacter metallireducens, which can transfer electrons to wild-type G. sulfurreducens via DIET, were established with a citrate synthase-deficient G. sulfurreducens strain that can receive electrons for respiration through DIET only. In a medium with ethanol as the electron donor and fumarate as the electron acceptor, co-cultures with the citrate synthase-deficient G. sulfurreducens strain metabolized ethanol as fast as co-cultures with wild-type, but the acetate that G. metallireducens generated from ethanol oxidation accumulated. The lack of acetate metabolism resulted in less fumarate reduction and lower cell abundance of G. sulfurreducens. RNAseq analysis of transcript abundance was consistent with a lack of acetate metabolism in G. sulfurreducens and revealed gene expression levels for the uptake hydrogenase, formate dehydrogenase, the pilus-associated c-type cytochrome OmcS and pili consistent with electron transfer via DIET. These results suggest that electrons transferred via DIET can serve as the sole energy source to support anaerobic respiration.

U2 - 10.1111/1758-2229.12093

DO - 10.1111/1758-2229.12093

M3 - Journal article

C2 - 24249299

VL - 5

SP - 904

EP - 910

JO - Environmental Microbiology Reports

JF - Environmental Microbiology Reports

SN - 1758-2229

IS - 6

ER -