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Research Article

Comparison of Single and Multiple Turnovers of SecYEG in Escherichia coli

Chunfeng Mao, Priya Bariya, Yuying Suo, Linda L. Randall
Thomas J. Silhavy, Editor
Chunfeng Mao
aDepartment of Biochemistry, University of Missouri, Columbia, Missouri, USA
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Priya Bariya
aDepartment of Biochemistry, University of Missouri, Columbia, Missouri, USA
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Yuying Suo
aDepartment of Biochemistry, University of Missouri, Columbia, Missouri, USA
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Linda L. Randall
aDepartment of Biochemistry, University of Missouri, Columbia, Missouri, USA
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  • ORCID record for Linda L. Randall
Thomas J. Silhavy
Princeton University
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DOI: 10.1128/JB.00462-20
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ABSTRACT

Precursor proteins are translocated across the cytoplasmic membrane in Escherichia coli by the general secretory, or Sec, pathway. The main components of the pathway are the integral membrane heterotrimeric SecYEG complex and the peripheral membrane ATPase, SecA. In this study, we have applied an in vitro assay using inverted cytoplasmic membrane vesicles to investigate the complex cycle that leads to translocation. We compared the apparent rate constants for nine precursors under two experimental conditions, single turnover and multiple turnovers. For each precursor, the rate constant for a single turnover was higher than for multiple turnovers, indicating that a different step limits the rate under the two conditions. We conclude that the rate-limiting step for a single turnover is an early step in the initial phase of transit through the channel, whereas the rate of multiple turnovers is limited by the resetting of the translocon. The presence of the chaperone SecB during multiple turnovers increased the maximal amplitude translocated for the three precursor species tested, pGBP, pPhoA, and proOmpA, and also increased the apparent rate constants for both pGBP and pPhoA. The rate constant for proOmpA was decreased by the presence of SecB.

IMPORTANCE Vastly different experimental techniques and conditions have been used to study export in E. coli. We demonstrated that altering experimental conditions can change the step that is observed during study. Investigators should consider specific experimental conditions when comparing data from different laboratories, as well as when comparing data from different experiments within a laboratory. We have shown that each precursor species has inherent properties that determine the translocation rate; thus generalizations from studies of a single species must be made with caution. A summary of advantages and disadvantages in use of nine precursors is presented.

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Comparison of Single and Multiple Turnovers of SecYEG in Escherichia coli
Chunfeng Mao, Priya Bariya, Yuying Suo, Linda L. Randall
Journal of Bacteriology Nov 2020, 202 (24) e00462-20; DOI: 10.1128/JB.00462-20

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Comparison of Single and Multiple Turnovers of SecYEG in Escherichia coli
Chunfeng Mao, Priya Bariya, Yuying Suo, Linda L. Randall
Journal of Bacteriology Nov 2020, 202 (24) e00462-20; DOI: 10.1128/JB.00462-20
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KEYWORDS

protein translocation
protein export
secretion
E. coli
SecA
SecYEG
translocon
single turnover
multiple turnovers
rate-limiting step

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