TY - JOUR
T1 - Diversification of Campylobacter jejuni Flagellar C-ring composition impacts its structure and function in motility, flagellar assembly, and cellular processes
AU - Henderson, Louie D.
AU - Matthews-Palmer, Teige R.S.
AU - Gulbronson, Connor J.
AU - Ribardo, Deborah A.
AU - Beeby, Morgan
AU - Hendrixson, David R.
N1 - Funding Information:
We thank Paul Simpson for assistance with electron microscopy. This work was supported by NIH grant R01AI065539 (to D.R.H.). C.J.G. was supported by NIH training grant T32 AI007520, L.D.H. was supported by a Biotechnology and Biological Sciences Research Council postgraduate training award, T.R.S.M.-P. was supported by the Francis Crick Institute (which receives its core funding from Cancer Research UK [FC001179], the UK Medical Research Council [FC001179], and the Wellcome Trust [FC001179]), and M.B. was supported by Medical Research Council grant MR/P019374/1.
Funding Information:
This work was supported by NIH grant R01AI065539 (to D.R.H.). C.J.G. was supported by NIH training grant T32 AI007520, L.D.H. was supported by a Biotechnology and Biological Sciences Research Council postgraduate training award, T.R.S.M.-P. was supported by the Francis Crick Institute (which receives its core funding from Cancer Research UK [FC001179], the UK Medical Research Council [FC001179], and the Wellcome Trust [FC001179]), and M.B. was supported by Medical Research Council grant MR/P019374/1.
Publisher Copyright:
© 2020 Henderson et al.
PY - 2020/1/1
Y1 - 2020/1/1
N2 - Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion. Some flagellar motors have diversified by recruiting additional components that influence torque and rotation, but little is known about the possible diversification and evolution of core motor components. The mechanistic core of flagella is the cytoplasmic C ring, which functions as a rotor, directional switch, and assembly platform for the flagellar type III secretion system (fT3SS) ATPase. The C ring is composed of a ring of FliG proteins and a helical ring of surface presentation of antigen (SPOA) domains from the switch proteins FliM and one of two usually mutually exclusive paralogs, FliN or FliY. We investigated the composition, architecture, and function of the C ring of Campylobacter jejuni, which encodes FliG, FliM, and both FliY and FliN by a variety of interrogative approaches. We discovered a diversified C. jejuni C ring containing FliG, FliM, and both FliY, which functions as a classical FliN-like protein for flagellar assembly, and FliN, which has neofunctionalized into a structural role. Specific protein interactions drive the formation of a more complex heterooligomeric C. jejuni C-ring structure. We discovered that this complex C ring has additional cellular functions in polarly localizing FlhG for numerical regulation of flagellar biogenesis and spatial regulation of division. Furthermore, mutation of the C. jejuni C ring revealed a T3SS that was less dependent on its ATPase complex for assembly than were other systems. Our results highlight considerable evolved flagellar diversity that impacts motor output, biogenesis, and cellular processes in different species.
AB - Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion. Some flagellar motors have diversified by recruiting additional components that influence torque and rotation, but little is known about the possible diversification and evolution of core motor components. The mechanistic core of flagella is the cytoplasmic C ring, which functions as a rotor, directional switch, and assembly platform for the flagellar type III secretion system (fT3SS) ATPase. The C ring is composed of a ring of FliG proteins and a helical ring of surface presentation of antigen (SPOA) domains from the switch proteins FliM and one of two usually mutually exclusive paralogs, FliN or FliY. We investigated the composition, architecture, and function of the C ring of Campylobacter jejuni, which encodes FliG, FliM, and both FliY and FliN by a variety of interrogative approaches. We discovered a diversified C. jejuni C ring containing FliG, FliM, and both FliY, which functions as a classical FliN-like protein for flagellar assembly, and FliN, which has neofunctionalized into a structural role. Specific protein interactions drive the formation of a more complex heterooligomeric C. jejuni C-ring structure. We discovered that this complex C ring has additional cellular functions in polarly localizing FlhG for numerical regulation of flagellar biogenesis and spatial regulation of division. Furthermore, mutation of the C. jejuni C ring revealed a T3SS that was less dependent on its ATPase complex for assembly than were other systems. Our results highlight considerable evolved flagellar diversity that impacts motor output, biogenesis, and cellular processes in different species.
KW - C ring
KW - Flagellar motor
KW - FlhG
KW - FliI
KW - FliN
KW - FliY
KW - Polar flagella
KW - Type III secretion
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UR - http://www.scopus.com/inward/citedby.url?scp=85077719376&partnerID=8YFLogxK
U2 - 10.1128/mBio.02286-19
DO - 10.1128/mBio.02286-19
M3 - Article
C2 - 31911488
AN - SCOPUS:85077719376
SN - 2161-2129
VL - 11
JO - mBio
JF - mBio
IS - 1
M1 - e02286-19
ER -