Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger

Herbert L. Axelrod, Debanu Das, Polat Abdubek, Tamara Astakhova, Constantina Bakolitsa, Dennis Carlton, Connie Chen, Hsiu Ju Chiu, Thomas Clayton, Marc C. Deller, Lian Duan, Kyle Ellrott, Carol L. Farr, Julie Feuerhelm, Joanna C. Grant, Anna Grzechnik, Gye Won Han, Lukasz Jaroszewski, Kevin K. Jin, Heath E. Klock & 28 others Mark W. Knuth, Piotr Kozbial, S. Sri Krishna, Abhinav Kumar, Winnie W. Lam, David Marciano, Daniel McMullan, Mitchell D. Miller, Andrew T. Morse, Edward Nigoghossian, Amanda Nopakun, Linda Okach, Christina Puckett, Ron Reyes, Natasha Sefcovic, Henry J. Tien, Christine B. Trame, Henry Van Den Bedem, Dana Weekes, Tiffany Wooten, Qingping Xu, Keith O. Hodgson, John Wooley, Marc André Elsliger, Ashley M. Deacon, Adam Godzik, Scott A. Lesley, Ian A. Wilson

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Examination of the genomic context for members of the FmdE Pfam family (PF02663), such as the protein encoded by the fmdE gene from the methanogenic archaeon Methanobacterium thermoautotrophicum, indicates that 13 of them are co-transcribed with genes encoding subunits of molybdenum formylmethanofuran dehydrogenase (EC 1.2.99.5), an enzyme that is involved in microbial methane production. Here, the first crystal structures from PF02663 are described, representing two bacterial and one archaeal species: B8FYU2-DESHY from the anaerobic dehalogenating bacterium Desulfito-bacterium hafniense DCB-2, Q2LQ23-SYNAS from the syntrophic bacterium Syntrophus aciditrophicus SB and Q9HJ63-THEAC from the thermoacidophilic archaeon Thermoplasma acidophilum. Two of these proteins, Q9HJ63-THEAC and Q2LQ23-SYNAS, contain two domains: an N-terminal thioredoxin-like α+Β core domain (NTD) consisting of a five-stranded, mixed Β-sheet flanked by several -helices and a C-terminal zinc-finger domain (CTD). B8FYU2-DESHY, on the other hand, is composed solely of the NTD. The CTD of Q9HJ63-THEAC and Q2LQ23-SYNAS is best characterized as a treble-clef zinc finger. Two significant structural differences between Q9HJ63-THEAC and Q2LQ23-SYNAS involve their metal binding. First, zinc is bound to the putative active site on the NTD of Q9HJ63-THEAC, but is absent from the NTD of Q2LQ23-SYNAS. Second, whereas the structure of the CTD of Q2LQ23-SYNAS shows four Cys side chains within coordination distance of the Zn atom, the structure of Q9HJ63-THEAC is atypical for a treble-cleft zinc finger in that three Cys side chains and an Asp side chain are within coordination distance of the zinc.

Original languageEnglish (US)
Pages (from-to)1335-1346
Number of pages12
JournalActa Crystallographica Section F: Structural Biology and Crystallization Communications
Volume66
Issue number10
DOIs
StatePublished - Oct 2010
Externally publishedYes

Fingerprint

Thioredoxins
Zinc Fingers
Zinc
zinc
charge transfer devices
Archaea
Bacteria
bacteria
Thermoplasma
Methanobacterium
genes
Molybdenum
Anaerobic Bacteria
Methane
Viperidae
Gene encoding
Genes
proteins
Catalytic Domain
Proteins

Keywords

  • domain swapping
  • metalloproteins
  • methanogenesis
  • Pfam family PF02663
  • structural genomics

ASJC Scopus subject areas

  • Biochemistry
  • Biophysics
  • Structural Biology
  • Genetics
  • Condensed Matter Physics

Cite this

Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger. / Axelrod, Herbert L.; Das, Debanu; Abdubek, Polat; Astakhova, Tamara; Bakolitsa, Constantina; Carlton, Dennis; Chen, Connie; Chiu, Hsiu Ju; Clayton, Thomas; Deller, Marc C.; Duan, Lian; Ellrott, Kyle; Farr, Carol L.; Feuerhelm, Julie; Grant, Joanna C.; Grzechnik, Anna; Han, Gye Won; Jaroszewski, Lukasz; Jin, Kevin K.; Klock, Heath E.; Knuth, Mark W.; Kozbial, Piotr; Krishna, S. Sri; Kumar, Abhinav; Lam, Winnie W.; Marciano, David; McMullan, Daniel; Miller, Mitchell D.; Morse, Andrew T.; Nigoghossian, Edward; Nopakun, Amanda; Okach, Linda; Puckett, Christina; Reyes, Ron; Sefcovic, Natasha; Tien, Henry J.; Trame, Christine B.; Van Den Bedem, Henry; Weekes, Dana; Wooten, Tiffany; Xu, Qingping; Hodgson, Keith O.; Wooley, John; Elsliger, Marc André; Deacon, Ashley M.; Godzik, Adam; Lesley, Scott A.; Wilson, Ian A.

In: Acta Crystallographica Section F: Structural Biology and Crystallization Communications, Vol. 66, No. 10, 10.2010, p. 1335-1346.

Research output: Contribution to journalArticle

Axelrod, HL, Das, D, Abdubek, P, Astakhova, T, Bakolitsa, C, Carlton, D, Chen, C, Chiu, HJ, Clayton, T, Deller, MC, Duan, L, Ellrott, K, Farr, CL, Feuerhelm, J, Grant, JC, Grzechnik, A, Han, GW, Jaroszewski, L, Jin, KK, Klock, HE, Knuth, MW, Kozbial, P, Krishna, SS, Kumar, A, Lam, WW, Marciano, D, McMullan, D, Miller, MD, Morse, AT, Nigoghossian, E, Nopakun, A, Okach, L, Puckett, C, Reyes, R, Sefcovic, N, Tien, HJ, Trame, CB, Van Den Bedem, H, Weekes, D, Wooten, T, Xu, Q, Hodgson, KO, Wooley, J, Elsliger, MA, Deacon, AM, Godzik, A, Lesley, SA & Wilson, IA 2010, 'Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger', Acta Crystallographica Section F: Structural Biology and Crystallization Communications, vol. 66, no. 10, pp. 1335-1346. https://doi.org/10.1107/S1744309110020166
Axelrod, Herbert L. ; Das, Debanu ; Abdubek, Polat ; Astakhova, Tamara ; Bakolitsa, Constantina ; Carlton, Dennis ; Chen, Connie ; Chiu, Hsiu Ju ; Clayton, Thomas ; Deller, Marc C. ; Duan, Lian ; Ellrott, Kyle ; Farr, Carol L. ; Feuerhelm, Julie ; Grant, Joanna C. ; Grzechnik, Anna ; Han, Gye Won ; Jaroszewski, Lukasz ; Jin, Kevin K. ; Klock, Heath E. ; Knuth, Mark W. ; Kozbial, Piotr ; Krishna, S. Sri ; Kumar, Abhinav ; Lam, Winnie W. ; Marciano, David ; McMullan, Daniel ; Miller, Mitchell D. ; Morse, Andrew T. ; Nigoghossian, Edward ; Nopakun, Amanda ; Okach, Linda ; Puckett, Christina ; Reyes, Ron ; Sefcovic, Natasha ; Tien, Henry J. ; Trame, Christine B. ; Van Den Bedem, Henry ; Weekes, Dana ; Wooten, Tiffany ; Xu, Qingping ; Hodgson, Keith O. ; Wooley, John ; Elsliger, Marc André ; Deacon, Ashley M. ; Godzik, Adam ; Lesley, Scott A. ; Wilson, Ian A. / Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger. In: Acta Crystallographica Section F: Structural Biology and Crystallization Communications. 2010 ; Vol. 66, No. 10. pp. 1335-1346.
@article{3291e072b66549ab9147d8847014ab11,
title = "Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger",
abstract = "Examination of the genomic context for members of the FmdE Pfam family (PF02663), such as the protein encoded by the fmdE gene from the methanogenic archaeon Methanobacterium thermoautotrophicum, indicates that 13 of them are co-transcribed with genes encoding subunits of molybdenum formylmethanofuran dehydrogenase (EC 1.2.99.5), an enzyme that is involved in microbial methane production. Here, the first crystal structures from PF02663 are described, representing two bacterial and one archaeal species: B8FYU2-DESHY from the anaerobic dehalogenating bacterium Desulfito-bacterium hafniense DCB-2, Q2LQ23-SYNAS from the syntrophic bacterium Syntrophus aciditrophicus SB and Q9HJ63-THEAC from the thermoacidophilic archaeon Thermoplasma acidophilum. Two of these proteins, Q9HJ63-THEAC and Q2LQ23-SYNAS, contain two domains: an N-terminal thioredoxin-like α+Β core domain (NTD) consisting of a five-stranded, mixed Β-sheet flanked by several -helices and a C-terminal zinc-finger domain (CTD). B8FYU2-DESHY, on the other hand, is composed solely of the NTD. The CTD of Q9HJ63-THEAC and Q2LQ23-SYNAS is best characterized as a treble-clef zinc finger. Two significant structural differences between Q9HJ63-THEAC and Q2LQ23-SYNAS involve their metal binding. First, zinc is bound to the putative active site on the NTD of Q9HJ63-THEAC, but is absent from the NTD of Q2LQ23-SYNAS. Second, whereas the structure of the CTD of Q2LQ23-SYNAS shows four Cys side chains within coordination distance of the Zn atom, the structure of Q9HJ63-THEAC is atypical for a treble-cleft zinc finger in that three Cys side chains and an Asp side chain are within coordination distance of the zinc.",
keywords = "domain swapping, metalloproteins, methanogenesis, Pfam family PF02663, structural genomics",
author = "Axelrod, {Herbert L.} and Debanu Das and Polat Abdubek and Tamara Astakhova and Constantina Bakolitsa and Dennis Carlton and Connie Chen and Chiu, {Hsiu Ju} and Thomas Clayton and Deller, {Marc C.} and Lian Duan and Kyle Ellrott and Farr, {Carol L.} and Julie Feuerhelm and Grant, {Joanna C.} and Anna Grzechnik and Han, {Gye Won} and Lukasz Jaroszewski and Jin, {Kevin K.} and Klock, {Heath E.} and Knuth, {Mark W.} and Piotr Kozbial and Krishna, {S. Sri} and Abhinav Kumar and Lam, {Winnie W.} and David Marciano and Daniel McMullan and Miller, {Mitchell D.} and Morse, {Andrew T.} and Edward Nigoghossian and Amanda Nopakun and Linda Okach and Christina Puckett and Ron Reyes and Natasha Sefcovic and Tien, {Henry J.} and Trame, {Christine B.} and {Van Den Bedem}, Henry and Dana Weekes and Tiffany Wooten and Qingping Xu and Hodgson, {Keith O.} and John Wooley and Elsliger, {Marc Andr{\'e}} and Deacon, {Ashley M.} and Adam Godzik and Lesley, {Scott A.} and Wilson, {Ian A.}",
year = "2010",
month = "10",
doi = "10.1107/S1744309110020166",
language = "English (US)",
volume = "66",
pages = "1335--1346",
journal = "Acta Crystallographica Section F:Structural Biology Communications",
issn = "1744-3091",
publisher = "John Wiley and Sons Ltd",
number = "10",

}

TY - JOUR

T1 - Structures of three members of Pfam PF02663 (FmdE) implicated in microbial methanogenesis reveal a conserved α+Β core domain and an auxiliary C-terminal treble-clef zinc finger

AU - Axelrod, Herbert L.

AU - Das, Debanu

AU - Abdubek, Polat

AU - Astakhova, Tamara

AU - Bakolitsa, Constantina

AU - Carlton, Dennis

AU - Chen, Connie

AU - Chiu, Hsiu Ju

AU - Clayton, Thomas

AU - Deller, Marc C.

AU - Duan, Lian

AU - Ellrott, Kyle

AU - Farr, Carol L.

AU - Feuerhelm, Julie

AU - Grant, Joanna C.

AU - Grzechnik, Anna

AU - Han, Gye Won

AU - Jaroszewski, Lukasz

AU - Jin, Kevin K.

AU - Klock, Heath E.

AU - Knuth, Mark W.

AU - Kozbial, Piotr

AU - Krishna, S. Sri

AU - Kumar, Abhinav

AU - Lam, Winnie W.

AU - Marciano, David

AU - McMullan, Daniel

AU - Miller, Mitchell D.

AU - Morse, Andrew T.

AU - Nigoghossian, Edward

AU - Nopakun, Amanda

AU - Okach, Linda

AU - Puckett, Christina

AU - Reyes, Ron

AU - Sefcovic, Natasha

AU - Tien, Henry J.

AU - Trame, Christine B.

AU - Van Den Bedem, Henry

AU - Weekes, Dana

AU - Wooten, Tiffany

AU - Xu, Qingping

AU - Hodgson, Keith O.

AU - Wooley, John

AU - Elsliger, Marc André

AU - Deacon, Ashley M.

AU - Godzik, Adam

AU - Lesley, Scott A.

AU - Wilson, Ian A.

PY - 2010/10

Y1 - 2010/10

N2 - Examination of the genomic context for members of the FmdE Pfam family (PF02663), such as the protein encoded by the fmdE gene from the methanogenic archaeon Methanobacterium thermoautotrophicum, indicates that 13 of them are co-transcribed with genes encoding subunits of molybdenum formylmethanofuran dehydrogenase (EC 1.2.99.5), an enzyme that is involved in microbial methane production. Here, the first crystal structures from PF02663 are described, representing two bacterial and one archaeal species: B8FYU2-DESHY from the anaerobic dehalogenating bacterium Desulfito-bacterium hafniense DCB-2, Q2LQ23-SYNAS from the syntrophic bacterium Syntrophus aciditrophicus SB and Q9HJ63-THEAC from the thermoacidophilic archaeon Thermoplasma acidophilum. Two of these proteins, Q9HJ63-THEAC and Q2LQ23-SYNAS, contain two domains: an N-terminal thioredoxin-like α+Β core domain (NTD) consisting of a five-stranded, mixed Β-sheet flanked by several -helices and a C-terminal zinc-finger domain (CTD). B8FYU2-DESHY, on the other hand, is composed solely of the NTD. The CTD of Q9HJ63-THEAC and Q2LQ23-SYNAS is best characterized as a treble-clef zinc finger. Two significant structural differences between Q9HJ63-THEAC and Q2LQ23-SYNAS involve their metal binding. First, zinc is bound to the putative active site on the NTD of Q9HJ63-THEAC, but is absent from the NTD of Q2LQ23-SYNAS. Second, whereas the structure of the CTD of Q2LQ23-SYNAS shows four Cys side chains within coordination distance of the Zn atom, the structure of Q9HJ63-THEAC is atypical for a treble-cleft zinc finger in that three Cys side chains and an Asp side chain are within coordination distance of the zinc.

AB - Examination of the genomic context for members of the FmdE Pfam family (PF02663), such as the protein encoded by the fmdE gene from the methanogenic archaeon Methanobacterium thermoautotrophicum, indicates that 13 of them are co-transcribed with genes encoding subunits of molybdenum formylmethanofuran dehydrogenase (EC 1.2.99.5), an enzyme that is involved in microbial methane production. Here, the first crystal structures from PF02663 are described, representing two bacterial and one archaeal species: B8FYU2-DESHY from the anaerobic dehalogenating bacterium Desulfito-bacterium hafniense DCB-2, Q2LQ23-SYNAS from the syntrophic bacterium Syntrophus aciditrophicus SB and Q9HJ63-THEAC from the thermoacidophilic archaeon Thermoplasma acidophilum. Two of these proteins, Q9HJ63-THEAC and Q2LQ23-SYNAS, contain two domains: an N-terminal thioredoxin-like α+Β core domain (NTD) consisting of a five-stranded, mixed Β-sheet flanked by several -helices and a C-terminal zinc-finger domain (CTD). B8FYU2-DESHY, on the other hand, is composed solely of the NTD. The CTD of Q9HJ63-THEAC and Q2LQ23-SYNAS is best characterized as a treble-clef zinc finger. Two significant structural differences between Q9HJ63-THEAC and Q2LQ23-SYNAS involve their metal binding. First, zinc is bound to the putative active site on the NTD of Q9HJ63-THEAC, but is absent from the NTD of Q2LQ23-SYNAS. Second, whereas the structure of the CTD of Q2LQ23-SYNAS shows four Cys side chains within coordination distance of the Zn atom, the structure of Q9HJ63-THEAC is atypical for a treble-cleft zinc finger in that three Cys side chains and an Asp side chain are within coordination distance of the zinc.

KW - domain swapping

KW - metalloproteins

KW - methanogenesis

KW - Pfam family PF02663

KW - structural genomics

UR - http://www.scopus.com/inward/record.url?scp=77958049996&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77958049996&partnerID=8YFLogxK

U2 - 10.1107/S1744309110020166

DO - 10.1107/S1744309110020166

M3 - Article

VL - 66

SP - 1335

EP - 1346

JO - Acta Crystallographica Section F:Structural Biology Communications

JF - Acta Crystallographica Section F:Structural Biology Communications

SN - 1744-3091

IS - 10

ER -