Pseudomonas Volume 6 Molecular Microbiology, Infection

and Biodiversity

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Juan-Luis Ramos · Alain Filloux
Editors

Pseudomonas

Volume 6: Molecular Microbiology, Infection

and Biodiversity

123
Editors
Prof. Juan-Luis Ramos Prof. Alain Filloux
Consejo Superior de Investigaciones Imperial College, London
Cientificas Faculty of Natural Science
c/Prof. Albareda, 1 Division of Cell & Molecular Biology
18008 Granada London
Spain South Kensington Campus
[email protected] Flowers Bldg.
United Kingdom SW7 2AZ

ISBN 978-90-481-3908-8 e-ISBN 978-90-481-3909-5

DOI 10.1007/978-90-481-3909-5
Springer Dordrecht Heidelberg London New York

Library of Congress Control Number: 2010921600

© Springer Science+Business Media B.V. 2010

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Preface

Paris is a cosmopolitan city where roaring life, wonderful museums and excellent
science can be found. It was during the XI IUMS conference held in this city
that the Pseudomonas book series was first envisaged. On the first row of the
auditorium sat a group of outstanding scientists in the field, who after devoting
much of their valuable time, contributed in an exceptional manner to the first three
volumes of the series, which saw the light simultaneously. The volumes were
grouped under the generic titles of “Vol. I. Pseudomonas: Genomics, Life Style
and Molecular Architecture”, Vol. II. Pseudomonas: Virulence and gene regulation;
Vol. III. Pseudomonas: Biosynthesis of Macromolecules and Molecular
Metabolism.
Soon after the completion of the first three volumes, a rapid search for arti-
cles containing the word Pseudomonas in the title in the last 10 years produced
over 6,000 articles! Consequently, not all possible topics relevant to this genus
were covered in the three first volumes. Since then two other volumes were pub-
lished: Pseudomonas volume IV edited by Roger Levesque and Juan L. Ramos that
came to being with the intention of collecting some of the most relevant emerging
new issues that had not been dealt with in the three previous volumes. This vol-
ume was arranged after the Pseudomonas meeting organized by Roger Levesque in
Quebec (Canada). It dealt with various topics grouped under a common heading:
“Pseudomonas: Molecular Biology of Emerging Issues”.
Yet the “Pseudomonas story” was far from complete and a new volume edited by
Juan L. Ramos and Alain Filloux was deemed necessary. The fifth volume was con-
ceived with the underlying intention of collecting new information on the genomics
of saprophytic soil Pseudomonas, as well as on the functions related to genomic
islands and was published in 2006.
At the request of a number of scientists and colleagues working in the field, we
have collected a new set of chapters that are called on to provide further views
on the biology of Pseudomonas. Chapters in Pseudomonas volume VI have been
grouped under the following topics: Regulation and control of virulence, Life styles,
Physiology and Metabolism. The chapters under the heading Life Styles constitute
an in-depth analysis of the genome of Pseudomonas stutzeri, a denitrifier par excel-
lence, and the behaviour and life style of P. aeruginosa in the human lung. The
Physiology Metabolism and Markers section collects four chapters that deal with the

v
vi Preface

metabolism of acyclic terpenes by Pseudomonas, the biodiversity of siderophores,

resistance to heavy metals and the role of relevant second messenger, a c-di-GMP, as
a signalling molecule. Finally under Regulation and control of virulence we find sev-
eral chapters dealing with sensing at the level of cell surfaces and quorum sensing,
as well as the role of small RNAs in the control of gene expression.
It would not be fair not to acknowledge that this sixth volume would never have
seen the light if it were not for a group of outstanding scientists in the field who
have produced enlightening chapters to try to complete the story that began with the
five previous volumes of the series. It has been an honour for us to work with them
and we truly thank them.
The review process has also been of great importance to ensure the high standards
of each chapter. Renowned scientists have participated in the review, correction and
editing of the chapters. Their assistance is immensely appreciated. We would like to
express our most sincere gratitude to:

Bonnie Bassler Norberto Palleroni

Burkhard Tümmler Paul Visca
Christophe Bordi Pierre Cornelis
Eduardo Díaz Regine Hennge-Aronis
Eric Deziel Simon Silver
Estrella Duque Soeren Molin
Hermann Heipieper Susanne Haussler
Iñigo Lasa Vittorio Venturi
Isabelle Schalk

We would also like to thank Carmen Lorente once again for her assistance and
enthusiasm in the compilation of the chapters that constitute this sixth volume.
Granada, Spain Juan L. Ramos
London, UK Alain Filloux
Contents

Part I Regulation and Control of Virulence

1 Small RNAs of Pseudomonas spp. . . . . . . . . . . . . . . . . . . . 3
Elisabeth Sonnleitner, Nicolas González and Dieter Haas
2 2-Alkyl-4(1H)-Quinolone Signalling in Pseudomonas aeruginosa . . 29
Matthew P. Fletcher, Stephan Heeb, Siri Ram Chhabra,
Stephen P. Diggle, Paul Williams, and Miguel Cámara
3 Cell-Surface Signalling in Pseudomonas . . . . . . . . . . . . . . . . 59
María A. Llamas and Wilbert Bitter
4 Second Messenger c-di-GMP Signaling in Pseudomonas aeruginosa 97
Massimo Merighi and Steve Lory

Part II Life Styles

5 Emergence of Pseudomonas aeruginosa in Cystic Fibrosis
Lung Infections . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
Joanna B. Goldberg
6 Insights into the Life Styles of Pseudomonas stutzeri . . . . . . . . . 177
Elena García-Valdés, Magdalena Mulet, and Jorge Lalucat

Part III Physiology, Metabolism and Markers

7 Pyoverdine Siderophores as Taxonomic and Phylogenic Markers . . 201
Jean-Marie Meyer
8 Metabolism of Acyclic Terpenes by Pseudomonas . . . . . . . . . . . 235
Jesús Campos-García
9 Heavy Metal Resistance in Pseudomonads . . . . . . . . . . . . . . . 255
Esther Aguilar-Barajas, Martha I. Ramírez-Díaz, Héctor
Riveros-Rosas, and Carlos Cervantes
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283

vii
Contributors

Esther Aguilar-Barajas Instituto de Investigaciones Químico-Biológicas,

Universidad Michoacana, UAM, Morelia, México
Wilbert Bitter Department of Medical Microbiology, VU University Medical
Centre, Amsterdam 1081 BT, The Netherlands
Miguel Cámara School of Molecular Medical Sciences, Centre for Biomolecular
Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK,
[email protected]
Jesús Campos-García Instituto de Investigaciones Químico-Biológicas,
Universidad Michoacana de San Nicolás de Hidalgo, Edif. B-3, Ciudad
Universitaria, CP 58030, Morelia, Michoacán, México, [email protected]
Carlos Cervantes Instituto de Investigaciones Químico-Biológicas, Universidad
Michoacana, UAM, Morelia, México, [email protected]
Siri Ram Chhabra School of Molecular Medical Sciences, Centre for
Biomolecular Sciences, University Park, University of Nottingham, Nottingham
NG7 2RD, UK
Stephen P. Diggle School of Molecular Medical Sciences, Centre for
Biomolecular Sciences, University Park, University of Nottingham, Nottingham
NG7 2RD, UK
Matthew P. Fletcher School of Molecular Medical Sciences, Centre for
Biomolecular Sciences, University Park, University of Nottingham, Nottingham
NG7 2RD, UK
Elena García-Valdés Microbiologia, Department de Biologia and IMEDEA
(CSIC-UIB), Universitat de les Illes Balears, Palma de Mallorca, Spain
Joanna B. Goldberg University of Virginia, Charlottesville, VA, USA,
[email protected]
Nicolas González Institut de Microbiologie, Centre Hospitalier Universitaire
Vaudois, CH-1011 Lausanne, Switzerland

ix
x Contributors

Dieter Haas Département de Microbiologie Fondamentale, Université de

Lausanne, CH-1015 Lausanne, Switzerland, [email protected]
Stephan Heeb School of Molecular Medical Sciences, Centre for Biomolecular
Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK
Jorge Lalucat Microbiologia, Department de Biologia and IMEDEA
(CSIC-UIB), Universitat de les Illes Balears, Palma de Mallorca, Spain,
[email protected]
María A. Llamas Department of Medical Microbiology, VU University Medical
Centre, Amsterdam 1081 BT, The Netherlands, [email protected]
Steve Lory Department of Microbiology and Molecular Genetics, Harvard
Medical School, Boston MA 02115, USA
Massimo Merighi Department of Microbiology and Molecular Genetics, Harvard
Medical School, Boston MA 02115, USA, [email protected]
Jean-Marie Meyer Département Génétique moléculaire, Génomique et
Microbiologie, UMR 7156 CNRS-Université de, Strasbourg, France,
[email protected]
Magdalena Mulet Microbiologia, Department de Biologia and IMEDEA
(CSIC-UIB), Universitat de les Illes Balears, Palma de Mallorca, Spain
Martha I. Ramírez-Díaz Instituto de Investigaciones Químico-Biológicas,
Universidad Michoacana, UAM, Morelia, México
Héctor Riveros-Rosas Departamento de Bioquímica, Facultad de Medicina,
UNAM, Mexico City, México
Elisabeth Sonnleitner Département de Microbiologie Fondamentale, Université
de Lausanne, CH-1015 Lausanne, Switzerland
Paul Williams School of Molecular Medical Sciences, Centre for Biomolecular
Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK
Obituary

Yoshifumi Itoh, Professor of Microbial Biotechnology at Tohoku University

(Sendai, Japan), suddenly passed away on October 4, 2008. He was well-known
to the Pseudomonas community as a specialist of amino acid metabolism and plas-
mid replication. In this book series, he contributed two chapters, one on arginine and
polyamine metabolism (in volume III) and one on histidine catabolism and catabo-
lite repression (in volume V). He published almost 100 papers and book chapters
during his career as a microbiologist.
Yoshi, as he was known to his friends, was born in a small city near Sendai
(Miyagi Prefecture) on August 5, 1951. Here he grew up with his elder sister
and younger brother. After studies at Tohoku University, he obtained a Master
of Agricultural Science in 1976 and a PhD of Agricultural Science in 1979. His
PhD thesis was on the mode of action of a bacteriocin in Erwinia carotovora. In

xi
xii Obituary

1980, he was hired as a Research Associate at Shinshu University (Matsumoto,

Japan), where he worked with Yoshiro Terawaki and Hideki Matsumoto. He soon
left to spend two years (1981–1983) as a postdoctoral fellow at the Department of
Microbiology, ETH Zurich (Switzerland) where he worked in the group of Thomas
Leisinger and Dieter Haas. He characterized the replication and partition functions
of the Pseudomonas plasmid pVS1. Many years later, in 2000, he extended this
work and, in collaboration with the group of Dieter Haas, made use of the mini-
mal pVS1 replicon in the construction of a series of stable plasmid vectors, which
are widely used and cited today. Upon return to Japan in 1983, he again joined
the School of Medicine at Shinshu University. In 1988, he moved to the National
Food Research Institute in Tsukuba where he eventually became the head of the
Applied Bacteriology Laboratory. He developed an interest in metabolic functions
of Pseudomonas aeruginosa and their regulation. Simultaneously, he also studied
Bacillus subtilis as an organism used for natto (fermented soybean) production.
In 2004, he became Director General of the Akita Research Institute of Food and
Brewing. At that time he was somewhat reluctant to take up this position, as it did
not allow him to spend much time on research. So he was very pleased that two years
later he was appointed to his home University at Sendai as a Professor. Although he
had substantial teaching commitments, he was finally able to return to his favourite
research topics.
Probably the most significant scientific contribution of Yoshifumi Itoh was his
discovery of the CbrAB two-component system in P. aeruginosa. This system reg-
ulates the activity of sigma-54 RNA polymerase during the utilization of numerous
carbon and nitrogen sources. Yoshifumi Itoh was a dedicated scientist and always
enthusiastic about his research. He had a fine sense of humour. His untimely death
came as a complete and very sad surprise to everyone. He is sorely missed by his
wife Junko, his daughter, his son and his friends and colleagues.
Dieter Haas
 Part I
Regulation and Control of Virulence
Chapter 1
Small RNAs of Pseudomonas spp.

Elisabeth Sonnleitner, Nicolas González and Dieter Haas

1.1 Introduction

Small RNAs (sRNAs) of prokaryotes are 40–600 nucleotides in length and most
have regulatory functions. As a rule, sRNAs do not encode polypeptides but impor-
tant exceptions exist. Some bacterial sRNAs were discovered and characterized in
the last two decades of the twentieth century, mostly with emphasis on sRNAs that
regulate functions of plasmids, bacteriophages or transposable elements. Although
it was already clear at that time that sRNAs could have diverse functions, their roles
as cellular regulators were not fully appreciated [1]. This picture has changed since
then with the discovery of many novel sRNAs, made possible by the introduction of
new computational and genomic approaches. To date, close to 100 sRNAs have been
reported in Escherichia coli and more than 150 sRNAs in prokaryotes altogether [2].
In this chapter, we will review the current status of sRNAs encoded by chromoso-
mal genes in Pseudomonas species, with emphasis on P. aeruginosa where most
genomic information is available. To date, > 40 sRNAs have been detected in this
organism; however, for many of them, the functions have not yet been uncovered.
Why has it been relatively difficult to find sRNAs and their genes in prokaryotes
by classical genetical and biochemical approaches? There are several reasons for
this. (i) Mutational inactivation of a particular sRNA gene often does not cause

D. Haas (B)
Département de Microbiologie Fondamentale, Université de Lausanne, CH-1015 Lausanne,
Switzerland
e-mail: [email protected]
Note added in proof:
After completion of this review in December 2008, Brencic et al. (Mol. Microbiol. 73:434–445,
2009) reported that the GacS/GacA two-component system achieves virtually all of its regulatory
effects by positively controlling the expression of the rsmY and rsmZ genes in P. aeruginosa, imply-
ing that the GacA protein binds exclusively to the rsmY and rsmZ promoters. Moreover, the global
H-NS-type regulator MvaT was recognised as a repressor of the rsmZ gene. Sonnleitner et al. (Proc.
Natl. Acad. Sci. USA, doi: 10.1073/pnas. 0910308106) described a novel sRNA, CrcZ, mediating
catabolite repression in P. aeruginosa. CrcZ is specified by the cbrB-pcnB intergenic region.

J.L. Ramos, A. Filloux (eds.), Pseudomonas, DOI 10.1007/978-90-481-3909-5_1, 3


C Springer Science+Business Media B.V. 2010
4 E. Sonnleitner et al.

an easily observable phenotype. (ii) Numerous sRNAs are functionally redun-

dant and therefore loss of one element does not have important consequences.
(iii) In transposon mutagenesis, sRNA genes may be spared because they are
small. (iv) Point mutations are much better tolerated in sRNA genes than in cod-
ing genes where missense, nonsense or frameshift mutations usually lead to loss
of function. (v) Overexpression of sRNAs, while providing a useful tool for prob-
ing sRNA function, is a technically demanding method in that it often requires a
strong external promoter to be fused precisely to the transcription start site of an
sRNA gene.
There are several strategies that have proved useful in the elucidation of prokary-
otic sRNAs. These approaches have been explored mostly in E. coli and several have
also been applied to Pseudomonas spp. (i) A few sRNAs are sufficiently abundant
so that they can be isolated from cells in pure form and sequenced. Historically,
this has been the case for 4.5S RNA (the product of the f f s gene, the RNA compo-
nent of the signal recognition particle), 6S RNA (the ssrS gene product, a regulator
of RNA polymerase), 10Sa RNA (the ssrA gene product, termed tmRNA today)
and 10Sb RNA (the rnpB product, the RNA component of RNase P) in E. coli [1].
However, most sRNAs are present in low amounts that preclude this approach. (ii)
Computational prediction of sRNAs, followed by experimental verification using
Northern blotting, has proved a broadly applicable strategy. Various algorithms have
been developed to this end. They usually assume that sRNA genes are located in
intergenic regions (IgRs) rather than within open reading frames and that putative
promoter and rho-independent terminator sequences must be within a short distance
of each other (< 500 nucleotides). Furthermore, computational predictions often
include the criterion that sequences as well as secondary structures of sRNAs should
be conserved in closely related bacterial species [3]. The principal limitation of this
approach is that it is difficult to predict bacterial promoters except for those that
have highly conserved RpoD, RpoN or RpoS recognition elements. Another limita-
tion is that in some cases no typical rho-independent terminator can be identified.
(iii) sRNAs that have a high affinity for an RNA-binding protein can often be co-
purified with the protein. Typically, the protein is isolated by immunoprecipitation
or affinity chromatography and cDNAs are prepared from the sRNAs attached to
the protein [4]. This strategy has been exploited successfully with proteins of the
Hfq and CsrA families. Here, an inconvenient feature is the fact that a large propor-
tion of non-specifically bound rRNAs and mRNA fragments are also enriched in the
purified protein fraction. At any rate, the roles of sRNAs recognized in (ii) or (iii)
have to be verified by genetic tests. (iv) Genetic screens – often involving multi-
copy expression of certain phenotypes – can be a fruitful strategy, especially when
post-transcriptional regulation of gene expression is suspected, as for example is the
case of the rpoS gene and genes encoding outer membrane proteins in E. coli [5–7].
Here, a caveat is that some overexpression effects might be missed because they are
slight and transient or toxic to the cell [8, 9]. (v) Transcripts emanating from IgRs
can be detected by microarrays when these cover the IgRs entirely; tiling microar-
rays are particularly useful in this respect. However, this approach can only be a