Phase Variation in Myxococcus xanthus Yields Cells Specialized for Iron Sequestration

Katarzyna Dziewanowska,Samuel Hunter,Patricia L Hartzell,Ingrid Linquist,Matthew Settles,Faye Schilkey,Paul Hoskisson

doi:10.1371/journal.pone.0095189

Katarzyna Dziewanowska, Samuel Hunter + Show 5 more

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https://doi.org/10.1371/journal.pone.0095189

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Abstract

Myxococcus xanthus undergoes phase variation during growth to produce predominantly two colony phenotypes. The majority are yellow colonies containing swarm-proficient cells and a minority are tan colonies containing swarm-deficient cells. Comparison of the transcriptomes of a yellow variant, a tan variant, and three tan mutants led to the identification of differentially-regulated genes that define key segments of the phase variation pathway. For example, expression of genes for the yellow pigment DKxanthene and the antibiotic myxovirescin was increased significantly in yellow variants. In contrast, expression of the siderophore myxochelin, hemin binding proteins, and iron transport proteins was increased specifically in tan strains. Thus, a consequence of phase variation is that yellow cells shift from producing antibiotic and pigment to producing components involved in acquisition of iron, which may increase fitness during periods of iron limitation. Multiple protein kinases and HTH-Xre DNA-binding proteins identified in this study may be involved in the regulatory hierarchy that governs phase variation.

Highlights

Phase variation (PV) is a form of phenotypic plasticity that allows a single bacterial species to persist in alternate forms by expressing different sets of genes
The redox versatility of this element accounts for its biological significance and contributes to problems with acquisition of iron. This is true for microbes such as M. xanthus that thrive in aerobic environments because Fe is very insoluble at neutral pH and in oxic environments
Most microbes produce extracellular ligands such as siderophores to sequester needed iron from the environment and have dedicated transport systems to bring Fe (III) siderophore complexes into the cell

Summary

Introduction

Phase variation (PV) is a form of phenotypic plasticity that allows a single bacterial species to persist in alternate forms by expressing different sets of genes. Organisms that undergo phase variation alter the expression of various cellular components via a genetic [1] or epigenetic [2,3] switch. The alternative programs result in production of different combinations of proteins, lipids, or carbohydrates on the cell surface that contribute to phase-specific changes in colony texture, color, or morphology [4]. Pathogenic strains that undergo PV produce cell types that are less likely to be recognized by the immune system, affording these pathogens enhanced opportunities to survive in the host. Photorhabdus luminescens produces M and P- morphotypes during phase variation. The M form is critical for the life cycle of P. luminescens because it is the form that can persist in the nematode host Heterorhabditis bacteriophora [5]

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