Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes

Qingping Xu, Bjørn A. Traag, Joost Willemse, Daniel McMullan, Mitchell D. Miller, Marc André Elsliger, Polat Abdubek, Tamara Astakhova, Herbert L. Axelrod, Constantina Bakolitsa, Dennis Carlton, Connie Chen, Hsiu Ju Chiu, Maksymilian Chruszcz, Thomas Clayton, Debanu Das, Marc C. Deller, Lian Duan, Kyle Ellrott, Dustin ErnstCarol L. Farr, Julie Feuerhelm, Joanna C. Grant, Anna Grzechnik, Slawomir K. Grzechnik, Gye Won Ha, Lukasz Jaroszewski, Kevin K. Jin, Heath E. Klock, Mark W. Knuth, Piotr Kozbial, S. Sri Krishna, Abhinav Kumar, David Marciano, Wladek Minor, A. Mieke Mommaas, Andrew T. Morse, Edward Nigoghossian, Amanda Nopakun, Linda Okach, Silvya Oommachen, Jessica Paulsen, Christina Puckett, Ron Reyes, Christopher L. Rife, Natasha Sefcovic, Henry J. Tien, Christine B. Trame, Henry van den Bedem, Shuren Wang, Dana Weekes, Keith O. Hodgson, John Wooley, Ashley M. Deacon, Adam Godzik, Scott A. Lesley, Ian A. Wilson, Gilles P. van Wezel

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

SsgA-like proteins (SALPs) are a family of homologous cell division-related proteins that occur exclusively in morphologically complex actinomycetes. We show that SsgB, a subfamily of SALPs, is the archetypal SALP that is functionally conserved in all sporulating actinomycetes. Sporulation-specific cell division of Streptomyces coelicolor ssgB mutants is restored by introduction of distant ssgB orthologues from other actinomycetes. Interestingly, the number of septa (and spores) of the complemented null mutants is dictated by the specific ssgB orthologue that is expressed. The crystal structure of the SsgB from Thermobifida fusca was determined at 2.6 Å resolution and represents the first structure for this family. The structure revealed similarities to a class of eukaryotic "whirly" single-stranded DNA/RNA-binding proteins. However, the electro-negative surface of the SALPs suggests that neither SsgB nor any of the other SALPs are likely to interact with nucleotide substrates. Instead, we show that a conserved hydrophobic surface is likely to be important for SALP function and suggest that proteins are the likely binding partners.

Original languageEnglish (US)
Pages (from-to)25268-25279
Number of pages12
JournalJournal of Biological Chemistry
Volume284
Issue number37
DOIs
StatePublished - Sep 11 2009
Externally publishedYes

Fingerprint

Actinobacteria
Cell Division
Cells
Proteins
Streptomyces coelicolor
RNA-Binding Proteins
DNA-Binding Proteins
Spores
Single-Stranded DNA
Protein Binding
Nucleotides
Crystal structure
Substrates

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes. / Xu, Qingping; Traag, Bjørn A.; Willemse, Joost; McMullan, Daniel; Miller, Mitchell D.; Elsliger, Marc André; Abdubek, Polat; Astakhova, Tamara; Axelrod, Herbert L.; Bakolitsa, Constantina; Carlton, Dennis; Chen, Connie; Chiu, Hsiu Ju; Chruszcz, Maksymilian; Clayton, Thomas; Das, Debanu; Deller, Marc C.; Duan, Lian; Ellrott, Kyle; Ernst, Dustin; Farr, Carol L.; Feuerhelm, Julie; Grant, Joanna C.; Grzechnik, Anna; Grzechnik, Slawomir K.; Ha, Gye Won; Jaroszewski, Lukasz; Jin, Kevin K.; Klock, Heath E.; Knuth, Mark W.; Kozbial, Piotr; Krishna, S. Sri; Kumar, Abhinav; Marciano, David; Minor, Wladek; Mommaas, A. Mieke; Morse, Andrew T.; Nigoghossian, Edward; Nopakun, Amanda; Okach, Linda; Oommachen, Silvya; Paulsen, Jessica; Puckett, Christina; Reyes, Ron; Rife, Christopher L.; Sefcovic, Natasha; Tien, Henry J.; Trame, Christine B.; van den Bedem, Henry; Wang, Shuren; Weekes, Dana; Hodgson, Keith O.; Wooley, John; Deacon, Ashley M.; Godzik, Adam; Lesley, Scott A.; Wilson, Ian A.; van Wezel, Gilles P.

In: Journal of Biological Chemistry, Vol. 284, No. 37, 11.09.2009, p. 25268-25279.

Research output: Contribution to journalArticle

Xu, Q, Traag, BA, Willemse, J, McMullan, D, Miller, MD, Elsliger, MA, Abdubek, P, Astakhova, T, Axelrod, HL, Bakolitsa, C, Carlton, D, Chen, C, Chiu, HJ, Chruszcz, M, Clayton, T, Das, D, Deller, MC, Duan, L, Ellrott, K, Ernst, D, Farr, CL, Feuerhelm, J, Grant, JC, Grzechnik, A, Grzechnik, SK, Ha, GW, Jaroszewski, L, Jin, KK, Klock, HE, Knuth, MW, Kozbial, P, Krishna, SS, Kumar, A, Marciano, D, Minor, W, Mommaas, AM, Morse, AT, Nigoghossian, E, Nopakun, A, Okach, L, Oommachen, S, Paulsen, J, Puckett, C, Reyes, R, Rife, CL, Sefcovic, N, Tien, HJ, Trame, CB, van den Bedem, H, Wang, S, Weekes, D, Hodgson, KO, Wooley, J, Deacon, AM, Godzik, A, Lesley, SA, Wilson, IA & van Wezel, GP 2009, 'Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes', Journal of Biological Chemistry, vol. 284, no. 37, pp. 25268-25279. https://doi.org/10.1074/jbc.M109.018564
Xu, Qingping ; Traag, Bjørn A. ; Willemse, Joost ; McMullan, Daniel ; Miller, Mitchell D. ; Elsliger, Marc André ; Abdubek, Polat ; Astakhova, Tamara ; Axelrod, Herbert L. ; Bakolitsa, Constantina ; Carlton, Dennis ; Chen, Connie ; Chiu, Hsiu Ju ; Chruszcz, Maksymilian ; Clayton, Thomas ; Das, Debanu ; Deller, Marc C. ; Duan, Lian ; Ellrott, Kyle ; Ernst, Dustin ; Farr, Carol L. ; Feuerhelm, Julie ; Grant, Joanna C. ; Grzechnik, Anna ; Grzechnik, Slawomir K. ; Ha, Gye Won ; Jaroszewski, Lukasz ; Jin, Kevin K. ; Klock, Heath E. ; Knuth, Mark W. ; Kozbial, Piotr ; Krishna, S. Sri ; Kumar, Abhinav ; Marciano, David ; Minor, Wladek ; Mommaas, A. Mieke ; Morse, Andrew T. ; Nigoghossian, Edward ; Nopakun, Amanda ; Okach, Linda ; Oommachen, Silvya ; Paulsen, Jessica ; Puckett, Christina ; Reyes, Ron ; Rife, Christopher L. ; Sefcovic, Natasha ; Tien, Henry J. ; Trame, Christine B. ; van den Bedem, Henry ; Wang, Shuren ; Weekes, Dana ; Hodgson, Keith O. ; Wooley, John ; Deacon, Ashley M. ; Godzik, Adam ; Lesley, Scott A. ; Wilson, Ian A. ; van Wezel, Gilles P. / Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes. In: Journal of Biological Chemistry. 2009 ; Vol. 284, No. 37. pp. 25268-25279.
@article{50bae48167aa42b1b9fde8b30be43581,
title = "Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes",
abstract = "SsgA-like proteins (SALPs) are a family of homologous cell division-related proteins that occur exclusively in morphologically complex actinomycetes. We show that SsgB, a subfamily of SALPs, is the archetypal SALP that is functionally conserved in all sporulating actinomycetes. Sporulation-specific cell division of Streptomyces coelicolor ssgB mutants is restored by introduction of distant ssgB orthologues from other actinomycetes. Interestingly, the number of septa (and spores) of the complemented null mutants is dictated by the specific ssgB orthologue that is expressed. The crystal structure of the SsgB from Thermobifida fusca was determined at 2.6 {\AA} resolution and represents the first structure for this family. The structure revealed similarities to a class of eukaryotic {"}whirly{"} single-stranded DNA/RNA-binding proteins. However, the electro-negative surface of the SALPs suggests that neither SsgB nor any of the other SALPs are likely to interact with nucleotide substrates. Instead, we show that a conserved hydrophobic surface is likely to be important for SALP function and suggest that proteins are the likely binding partners.",
author = "Qingping Xu and Traag, {Bj{\o}rn A.} and Joost Willemse and Daniel McMullan and Miller, {Mitchell D.} and Elsliger, {Marc Andr{\'e}} and Polat Abdubek and Tamara Astakhova and Axelrod, {Herbert L.} and Constantina Bakolitsa and Dennis Carlton and Connie Chen and Chiu, {Hsiu Ju} and Maksymilian Chruszcz and Thomas Clayton and Debanu Das and Deller, {Marc C.} and Lian Duan and Kyle Ellrott and Dustin Ernst and Farr, {Carol L.} and Julie Feuerhelm and Grant, {Joanna C.} and Anna Grzechnik and Grzechnik, {Slawomir K.} and Ha, {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 David Marciano and Wladek Minor and Mommaas, {A. Mieke} and Morse, {Andrew T.} and Edward Nigoghossian and Amanda Nopakun and Linda Okach and Silvya Oommachen and Jessica Paulsen and Christina Puckett and Ron Reyes and Rife, {Christopher L.} and Natasha Sefcovic and Tien, {Henry J.} and Trame, {Christine B.} and {van den Bedem}, Henry and Shuren Wang and Dana Weekes and Hodgson, {Keith O.} and John Wooley and Deacon, {Ashley M.} and Adam Godzik and Lesley, {Scott A.} and Wilson, {Ian A.} and {van Wezel}, {Gilles P.}",
year = "2009",
month = "9",
day = "11",
doi = "10.1074/jbc.M109.018564",
language = "English (US)",
volume = "284",
pages = "25268--25279",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "37",

}

TY - JOUR

T1 - Structural and functional characterizations of SsgB, a conserved activator of developmental cell division in morphologically complex actinomycetes

AU - Xu, Qingping

AU - Traag, Bjørn A.

AU - Willemse, Joost

AU - McMullan, Daniel

AU - Miller, Mitchell D.

AU - Elsliger, Marc André

AU - Abdubek, Polat

AU - Astakhova, Tamara

AU - Axelrod, Herbert L.

AU - Bakolitsa, Constantina

AU - Carlton, Dennis

AU - Chen, Connie

AU - Chiu, Hsiu Ju

AU - Chruszcz, Maksymilian

AU - Clayton, Thomas

AU - Das, Debanu

AU - Deller, Marc C.

AU - Duan, Lian

AU - Ellrott, Kyle

AU - Ernst, Dustin

AU - Farr, Carol L.

AU - Feuerhelm, Julie

AU - Grant, Joanna C.

AU - Grzechnik, Anna

AU - Grzechnik, Slawomir K.

AU - Ha, 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 - Marciano, David

AU - Minor, Wladek

AU - Mommaas, A. Mieke

AU - Morse, Andrew T.

AU - Nigoghossian, Edward

AU - Nopakun, Amanda

AU - Okach, Linda

AU - Oommachen, Silvya

AU - Paulsen, Jessica

AU - Puckett, Christina

AU - Reyes, Ron

AU - Rife, Christopher L.

AU - Sefcovic, Natasha

AU - Tien, Henry J.

AU - Trame, Christine B.

AU - van den Bedem, Henry

AU - Wang, Shuren

AU - Weekes, Dana

AU - Hodgson, Keith O.

AU - Wooley, John

AU - Deacon, Ashley M.

AU - Godzik, Adam

AU - Lesley, Scott A.

AU - Wilson, Ian A.

AU - van Wezel, Gilles P.

PY - 2009/9/11

Y1 - 2009/9/11

N2 - SsgA-like proteins (SALPs) are a family of homologous cell division-related proteins that occur exclusively in morphologically complex actinomycetes. We show that SsgB, a subfamily of SALPs, is the archetypal SALP that is functionally conserved in all sporulating actinomycetes. Sporulation-specific cell division of Streptomyces coelicolor ssgB mutants is restored by introduction of distant ssgB orthologues from other actinomycetes. Interestingly, the number of septa (and spores) of the complemented null mutants is dictated by the specific ssgB orthologue that is expressed. The crystal structure of the SsgB from Thermobifida fusca was determined at 2.6 Å resolution and represents the first structure for this family. The structure revealed similarities to a class of eukaryotic "whirly" single-stranded DNA/RNA-binding proteins. However, the electro-negative surface of the SALPs suggests that neither SsgB nor any of the other SALPs are likely to interact with nucleotide substrates. Instead, we show that a conserved hydrophobic surface is likely to be important for SALP function and suggest that proteins are the likely binding partners.

AB - SsgA-like proteins (SALPs) are a family of homologous cell division-related proteins that occur exclusively in morphologically complex actinomycetes. We show that SsgB, a subfamily of SALPs, is the archetypal SALP that is functionally conserved in all sporulating actinomycetes. Sporulation-specific cell division of Streptomyces coelicolor ssgB mutants is restored by introduction of distant ssgB orthologues from other actinomycetes. Interestingly, the number of septa (and spores) of the complemented null mutants is dictated by the specific ssgB orthologue that is expressed. The crystal structure of the SsgB from Thermobifida fusca was determined at 2.6 Å resolution and represents the first structure for this family. The structure revealed similarities to a class of eukaryotic "whirly" single-stranded DNA/RNA-binding proteins. However, the electro-negative surface of the SALPs suggests that neither SsgB nor any of the other SALPs are likely to interact with nucleotide substrates. Instead, we show that a conserved hydrophobic surface is likely to be important for SALP function and suggest that proteins are the likely binding partners.

UR - http://www.scopus.com/inward/record.url?scp=69949145448&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=69949145448&partnerID=8YFLogxK

U2 - 10.1074/jbc.M109.018564

DO - 10.1074/jbc.M109.018564

M3 - Article

C2 - 19567872

AN - SCOPUS:69949145448

VL - 284

SP - 25268

EP - 25279

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 37

ER -