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Title: Phosphorylation of spore coat proteins by a family of atypical protein kinases

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [2];  [1];  [3];  [4];  [5];  [6];  [2];  [3];  [7];  [5];  [8];  [2]
  1. Univ. of California, San Diego, CA (United States). Dept. of Pharmacology
  2. Univ. of Texas Southwestern Medical Center, Dallas, TX (United States). Dept. of Molecular Biology
  3. Univ. of California, San Diego, CA (United States). Division of Biological Sciences
  4. Polish Academy of Sciences (PAS), Warsaw (Poland). Inst. of Biochemistry and Biophysics. Dept. of Microbial Biochemistry
  5. Warsaw Univ. of Life Sciences (Poland). Dept. of Experimental Design and Bioinformatics
  6. Polish Academy of Sciences (PAS), Warsaw (Poland). Inst. of Biochemistry and Biophysics. Dept. of Biophysics
  7. Univ. of Texas Southwestern Medical Center, Dallas, TX (United States). Dept. of Biophysics and Biochemistry
  8. Univ. of California, San Diego, CA (United States). Dept. of Pharmacology. Dept. of Cellular and Molecular Medicine. Dept. of Chemistry and Biochemistry

The modification of proteins by phosphorylation occurs in all life forms and is catalyzed by a large superfamily of enzymes known as protein kinases. We recently discovered a family of secretory pathway kinases that phosphorylate extracellular proteins. One member, family with sequence similarity 20C (Fam20C), is the physiological Golgi casein kinase. While examining distantly related protein sequences, we observed low levels of identity between the spore coat protein H (CotH), and the Fam20C-related secretory pathway kinases. CotH is a component of the spore in many bacterial and eukaryotic species, and is required for efficient germination of spores in Bacillus subtilis; however, the mechanism by which CotH affects germination is unclear. In this paper, we show that CotH is a protein kinase. The crystal structure of CotH reveals an atypical protein kinase-like fold with a unique mode of ATP binding. Examination of the genes neighboring cotH in B. subtilis led us to identify two spore coat proteins, CotB and CotG, as CotH substrates. Furthermore, we show that CotH-dependent phosphorylation of CotB and CotG is required for the efficient germination of B. subtilis spores. Finally and collectively, our results define a family of atypical protein kinases and reveal an unexpected role for protein phosphorylation in spore biology.

Research Organization:
Univ. of California, San Diego, CA (United States); Univ. of Texas Southwestern Medical Center, Dallas, TX (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States); Polish National Science Centre (Poland)
Contributing Organization:
Polish Academy of Sciences (PAS), Warsaw (Poland); Warsaw Univ. of Life Sciences (Poland)
Grant/Contract Number:
AC02-06CH11357; DK018849; DK018024; R00DK099254; GM57045; 2012/05/B/NZ3/00413; 2012/07/D/NZ2/04286; RR150033
OSTI ID:
1274751
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 25; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
ENGLISH
Citation Metrics:
Cited by: 42 works
Citation information provided by
Web of Science

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Cited By (13)

Discovery and characterization of a Gram-positive Pel polysaccharide biosynthetic gene cluster journal April 2020
Phosphoproteomic insights into processes influenced by the kinase-like protein DIA1/C3orf58 journal January 2018
Progress in research and application development of surface display technology using Bacillus subtilis spores journal January 2020
PEAK3/C19orf35 pseudokinase, a new NFK3 kinase family member, inhibits CrkII through dimerization journal July 2019
Discovery and characterization of a Gram-positive Pel polysaccharide biosynthetic gene cluster posted_content September 2019
Dynamic sporulation gene co-expression networks for Bacillus subtilis 168 and the food-borne isolate Bacillus amyloliquefaciens: a transcriptomic model journal February 2018
A parts list for fungal cellulosomes revealed by comparative genomics journal May 2017
Thinking outside of the cell: Secreted protein kinases in bacteria, parasites, and mammals journal April 2019
IL-1 Fragment Modulates Immune Response Elicited by Recombinant Bacillus subtilis Spores Presenting an Antigen/Adjuvant Chimeric Protein journal September 2018
Bacillus subtilis builds structurally and functionally different spores in response to the temperature of growth journal November 2019
Conidial surface proteins at the interface of fungal infections journal September 2019
Accumulation and Release of Rare Earth Ions by Spores of Bacillus Species and the Location of These Ions in Spores journal June 2019
Protein post-translational modifications in bacteria journal September 2019

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