Operon Gene Order Is Optimized for Ordered Protein Complex Assembly.

Joseph A. Marsh,Jonathan N. Wells,L. Therese Bergendahl

doi:10.1016/j.celrep.2015.12.085

Abstract

SummaryThe assembly of heteromeric protein complexes is an inherently stochastic process in which multiple genes are expressed separately into proteins, which must then somehow find each other within the cell. Here, we considered one of the ways by which prokaryotic organisms have attempted to maximize the efficiency of protein complex assembly: the organization of subunit-encoding genes into operons. Using structure-based assembly predictions, we show that operon gene order has been optimized to match the order in which protein subunits assemble. Exceptions to this are almost entirely highly expressed proteins for which assembly is less stochastic and for which precisely ordered translation offers less benefit. Overall, these results show that ordered protein complex assembly pathways are of significant biological importance and represent a major evolutionary constraint on operon gene organization.

Highlights

The assembly of proteins into complexes is integral to a wide range of biological processes
We have extensive knowledge of the diverse quaternary structures formed by protein complexes (Goodsell and Olson, 2000; Janin et al, 2008; Marsh and Teichmann, 2015; Ahnert et al, 2015), much less is known about how they assemble and how assembly is regulated
Advances in electrospray mass spectrometry techniques have provided major new insights into in vitro assembly, allowing the assembly and disassembly pathways of protein complexes with diverse quaternary structure topologies to be elucidated in detail (Hernandez and Robinson, 2007)

Summary

Graphical Abstract

Many prokaryotic protein complexes are operon-encoded, so that subunits of the same complex will be translated from the same mRNA. Wells et al show that the order in which genes are arranged in operons tends to be optimized for the order in which protein complex subunits assemble.

SUMMARY

INTRODUCTION

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EXPERIMENTAL PROCEDURES