Microbial ecology of aerial plant surfaces

347 Pages·2006·7.513 MB·English

by  Mark J Bailey, Centre for Ecology & Hydrology, Oxford., et al

Microbial Ecology of Aerial Plant Surfaces
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Microbial Ecology of Aerial
Plant Surfaces
Edited by
M.J. Bailey
Centre for Ecology and Hydrology, Mansfield Road,
Oxford, UK
A.K. Lilley
Centre for Ecology and Hydrology, Mansfield Road,
Oxford, UK
T.M. Timms-Wilson
Centre for Ecology and Hydrology, Mansfield Road,
Oxford, UK
and
P.T.N. Spencer-Phillips
School of Biosciences, University of the West of
England, Coldharbour Lane, Bristol, UK.
www.cabi.org
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© CAB International 2006. All rights reserved. No part of this publication
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copyright owners.
A catalogue record for this book is available from the British Library, London,
UK.
A catalogue record for this book is available from the Library of Congress,
Washington, DC.
ISBN-10: 1 84593 061 4
ISBN-13: 9781 84593061 5
Printed and bound in the UK from copy supplied by the editors by Athenaeum Press,
Gateshead.
Contents
Preface viii
Contributors xiv
Section I: Biodiversity and Population Genetics
of Phyllosphere Communities
1. Phyllosphere Microbiology: A Perspective 1
S. Lindow
2. Microbial Diversity in the Phyllosphere and Rhizosphere
of Field Grown Crop Plants: Microbial Specialisation at
the Plant Surface 21
T.M. Timms-Wilson, K. Smalla, T.I. Goodall, A. Houlden,
V. GallegoandM.J. Bailey
3. Diversity, Scale and Variation of Endophytic Fungi in
Leaves of Tropical Plants 37
P. Bay man
4. Microorganisms in the Phyllosphere of Temperate Forest
Ecosystems in a Changing Environment 51
T. Milller, K. Strobel and A. Ulrich
Section II: Spatial Distribution and Biofilms
5. Bacterial Biofilm Formation, Adaptation and Fitness 67
S. Rice and S. Kjelleberg
6. Bacterial Assemblages on Plant Surfaces 83
J.-M. Monier
7. The Role of Plant Genetics in Determining Above- and
Below-ground Microbial Communities 107
J.A. Schweitzer, J.K. Bailey, R.K. Bangert, S.C. Hart
and T.G. Whitham
8. A Survey of A-L Biofilm Formation and Cellulose
Expression Amongst Soil and Plant-Associated
Pseudomonas Isolates 121
A.J. Spiers, D.L. Arnold, C.D. Moon and
T.M. Timms-Wilson
Section III: Biological Control and Pathogenicity
9. Biological Control of Plant Diseases by Phyllosphere
Applied Biological Control Agents 133
B.J. Jacobsen
10. Ecophysiology of Biocontrol Agents for Improved
Competence in the Phyllosphere 149
N. Magan
11. Compost Teas: Alternative Approaches to the
Biological Control of Plant Diseases 165
W.F. Mahaffee and S.J. Scheuerell
Section IV: Gene Expression and Phyllosphere Genomics
12. Molecular Interactions at the Leaf Surface:
Xanthomonas and its Host 181
M. Wilson, W. Moss, Y. Zhang and J. Jones
13. Erwiniae: Genomics and the Secret Life of a
Plant Pathogen 191
I.K. Toth, L. Moleleki, L. Pritchard, H. Liu, S. Humphris,
L. Hyman, G.W. Axelsen, M.B. Brurberg, M. Ravensdale,
E. Gilroy and P.R. J. Birch
14. Host-Pathogen Interactions of Relevance to the
Phyllosphere 201
G.W. Sundin
Section V: Leaf Colonisation and Dispersal
15. Effects of Endophytes on Colonisation by Leaf
Surface Microbiota 209
R.W.S. Weber and H. Anke
16. Plant Control of Phyllosphere Diversity: Genotype
Interactions with Ultraviolet-B Radiation 223
A.E. Stapleton and S.J. Simmons
17. Population Growth and the Landscape Ecology of
Microbes on Leaf Surfaces 239
J.H. Andrews
18. What DNA Microarrays Can Tell Us About Bacterial
Diversity: A New Light on an Old Question 251
G.L. Andersen, Y.M. Piceno, T.Z. DeSantis and E.L. Brodie
vi
Section VI: Aerobiology and Plant Surface Microbiology
19. Human Pathogens and the Health Threat of the
Phyllosphere 269
M.T. Brandl
20. Post-harvest Spoilage of Wheat Grains: Malodour
Formation and the Infection Process 287
P.T.N. Spencer-Phillips, A. Wallington, W. Kockenberger,
H.E. Gunson and N.M. Ratcliffe
21. Atmospheric Composition and the Phyllosphere:
The Role of Foliar Surfaces in Regulating
Biogeochemical Cycles 304
D. Fowler, J.N. Cape, J. Muller, M. Coyle, M.A. Sutton,
R. Smith and C. Jeffree
Index 316
The colour plate section is inserted after p.238
PREFACE
In July 2005, the Centre of Ecology and Hydrology, Oxford (CEH-Oxford) hosted an
International Symposium on the Microbiology of Aerial Plant Surfaces at St Catherine's
College, Oxford. This was the eighth in this series of meetings which have been held every
five years since 1970. The symposia bring together scientists studying the biology and
ecology of the microbiology of the surfaces of above ground, aerial portion of vascular
plants (stem, leaves, fruit, flowers, etc.) collectively known as the phylloplane. The
presentations, discussions and the following chapters developed from this meeting,
Phyllosphere 2005, highlight both the value of this highly diverse habitat to research in
microbiology and the importance of this research to plant health and ecosystem functions.
The abundance of life in the phyllosphere is matched by the habitat range that plants
occupy in both terrestrial and aquatic environments. Plant leaves provide the greatest
surface area on the planet, tolerating geographic and climatic extremes that can fluctuate on
a daily cycle from sub-zero night time temperatures to leaf surface temperatures that exceed
50°C in direct sunlight. Plants are found on over 90% of the approximately 2 x 108 km2 of
terrestrial surface of the planet. The total surface area of leaves for terrestrial plants may
approach one billion square kilometres (1 x 109 km2). Microorganisms (bacteria, fungi,
archaea, protists) that have adapted to life in the phyllosphere must exhibit a range of
phenotypic characteristics to mitigate against the effect of these physical parameters. These
are perhaps greater than those experienced, for example, by soil or rhizosphere bacteria
where temperatures, moisture content and nutrient availability are fairly constant when
compared to the phyllosphere. Resource limitation, in respect to nutrient supply and water
availability, are common selective factors that dictate the range and functional capacity of
microbial life at plant surfaces. To understand more about the wider context of the
microbiology of plant associated habitats, we would recommend that you also draw on the
published proceedings of the other symposia on phyllosphere microbiology and of the
chapters that follow.
The surface and interior of aerial parts of plants, including flowers, fruits, stems and
leaves represent the phyllosphere. Specialised microbial colonists, phytopathogens,
spoilage and plant protecting organisms as well as periodic immigrants have all been
described for this diverse habitat. As plants represent one of the most important features of
our landscape and our primary food source it is somewhat surprising that only a limited
number of detailed investigations have been conducted that describe their above-ground
microbiology. This is in stark contrast to the attention that soil rhizosphere systems receive.
Pertinent investigations reveal a diverse and specialised microbial community that is
distinct from the rhizosphere. Bacteria are by far the most numerically abundant colonisers
of the phyllosphere, and typical community densities in the order of 2 xl O7 cells per cm2 of
leaf surface have been recorded, although these numbers can vary from as little as 10s to in
excess of 1 x 1012 in arid and senescing leaves respectively. Densities vary over the plant
surface, in leaf buds or on young emerging leaves densities may be two orders of
magnitude greater than those estimated in established mature leaves. These differences can
be explained in part by the increased availability of water as these regions are often
protected or collect moisture derived from rainfall or dew. In addition, nutrient loss from
young, developing leaves provides suitable carbon (C) and nitrogen (N) sources for
colonising bacteria which can form complex mixed assemblages or biofilms that facilitate
survival. These assemblages also represent suites of significant bacterial activity and
horizontal gene transfer. The source of these primary colonists remains somewhat obscure
viii
but in studies of developing seedlings the bacteria identified are often typical of those also
found in the spermosphere and in rhizosphere soils. As plants develop, the phyllosphere
community develops and becomes distinct, both in terms of relative abundance and
complexity, from that found in the below-ground environment. Bacteria are often the focus
of phyllosphere study as they are reported to be the numerically most abundant of isolates
recorded using both isolation and culture independent methods. These general observations
however are not intended to imply that yeasts and other fungi have a less important role.
Section I of this book concerns the biodiversity and population genetics of
phyllosphere communities. The aerial portion of plants supports a diversity of
microorganisms, including bacteria, fungi and archaea. As the following chapters reveal,
there has been a major advance in the study of leaf surface organisms. The development of
molecular tools has allowed the accurate description of the microbial diversity of many
environments based on gene analyses and comparison. Specific measures of gene
expression are reported, not only based on the assessment of messenger RNA expression
but also through the analysis of protein synthesis using antibody assays or the direct
assessment of function. Furthermore with the use of reporter genes that fluoresce, emit
light or produce an enzyme that catabolises the production of colorimetric substrates, it is
now possible to record how individual cells perceive and respond to their environment.
Methods based on the polymerase chain reaction (PCR) include amplified ribosomal
DNA restriction analysis (ARDRA), terminal restriction fragment length polymorphism (T-
RFLP), and length heterogeneity or LH-PCR which are all based on enzymic digestion of
PCR derived amplimers with restriction endonuclease enzymes. Denaturing gradient gel
electrophoretic (DGGE) analysis of the products of PCR amplified 16S and 18S rRNA
genes has been applied to describe the total diversity of phyllosphere communities.
Unsurprisingly this reveals that many previously described bacterial genera are indeed
abundant, but interestingly only a few novel taxa were detected.
Some studies are beginning to integrate a variety of sampling methods to produce
more integrated views of the phyllosphere microbial community structure. In Chapter 2,
Timms-Wilson and colleagues report on the use of a variety of methods to assay changes in
bacterial and fungal community structure and function on three field grown crop plants
through a growing season. These methods include standard culture based and non-culture
based analyses, including use of selective plate counts on microbiological agars for bacteria
and fungi, community level physiological profiling (CLPP) with BIOLOG plates
containing a range of sole carbon sources to analyse the 'metabolic potential' of responsive
bacterial communities and PCR-DGGE of 16S and 18S ribosomal RNA genes to assess
"total" diversity for bacteria and fungi.
Progress in the development of appropriate and representative sampling methods
continues to play a major role in improving our understanding of microbial diversity. In
Chapter 3, Bayman elegantly describes how different sampling strategies affect the
diversity recorded in tropical and temperate phyllosphere bacterial and fungal communities.
The chapter demonstrates considerable leaf-to-leaf variation in diversity and between
adjacent epiphyte and endophyte biotas. Of particular note is the observation that a
reduction in the size of the leaf fragment sampled leads to substantial increases in the
diversity of fungi detected. Bayman proposes, where practical, that the selection of an
optimal sample size of leaf fragment, for example one that contains a single colony, may
avoid the inhibitory effects of different populations on one another.
Phyllosphere biodiversity studies are moving from investigation of populations and
communities to experimentation on their role in global ecology. The phyllosphere of the
temperate forest tree canopy is a substantial habitat which can influence regional and global
ecosystem cycling. Environmental changes in climate, CO levels, UV radiation and air
2
pollutants all affect the phyllosphere microbial populations which in turn can exhibit altered
growth and activity. In Chapter 4, Milller and colleagues report the effects of
environmental change on the ecosystems of the temperate forest phyllosphere. This
habitat is the site of microbial activity transforming organic matter and affecting nutrient
cycling. The authors consider this activity, the effects of air pollution and insect invasions
on forest ecosystems. They show that phylloplane microbial community activity may be
enhanced by invasive insect species, which may grow better when plants are stressed by
atmospheric pollutants. Such combined responses can lead to elevated nutrient cycling in
the canopies of forest trees with higher organic matter and energy flow from the canopy to
the forest floor.
Section II of this book concerns the spatial distribution and biofllm structures of
microbes on the phylloplane. Technological advances have facilitated the direct surface
imaging of the distribution and activity of key groups. These methods have facilitated real
progress in the understanding of bacterial biofilm formation in many habitats. In Chapter 5,
Rice and Kjelleberg provide a comprehensive review of the progress in methods, models
and the understanding of the formation of bacterial biofilms. They stress the roles of
signalling and biofilm formation in bacterial adaptation and fitness. On the phylloplane,
these are important factors in the interaction of bacteria with plants and microbial
eukaryotes.
Studies of bacterial phyllosphere communities have often shown that many bacteria
are present as solitary cells, although the majority are highly aggregated in large
assemblages embedded in an exopolymeric matrix. In Chapter 6, Monier reports on studies
of these high density multi-population aggregates by integrating molecular methods and
light microscopy. These studies have confirmed that bacterial phylloplane activity shows a
variety of density-dependent traits where leaf surface colonisation involves a high level of
spatial segregation. Understanding of interactions at the micro scale is providing important
biological and ecological insights.
Moving to a new level of spatial scale and interaction, in Chapter 7, Schweitzer and
colleagues examine the role that plant genetics play in determining both phyllosphere and
rhizosphere microbial communities. It is proposed that the genetics of a host plant are an
important common factor that can impact diverse communities which provides a plant-
related basis to ecological and evolutionary processes.
Bacterial biofilms in soil and plant habitats use a variety of extracellular
polysaccharides (EPS) initially for attachment and then to provide a matrix for colonisation.
In Chapter, 8 Spiers and colleagues survey biofilm formation and cellulose expression
amongst soil and plant-associated pseudomonads. Partially acetylated cellulose has been
implicated in biofilm formation and successful phytosphere colonisation by the plant
growth promoting rhizobacteria, PGPR Pseudomonas fluorescens SBW25.
Section III of this book concerns biological control and pathogenicity. Plant
protection from pathogens using biological control is today a common component in crop
protection. In Chapter 9, Jacobsen reviews the use of bacteria and fungi against a variety of
plant diseases and pests. Successful biological control agents (BCAs) need to be produced
with appropriate formulation, shelf-life and reproducibility of performance in the
phyllosphere. Magan's Chapter 10 considers the use of physiological manipulation of the
growth of fungal BCAs. Specific growth and formulation of inoculum has the potential to
enhance the synthesis of nutrient reserves which can be exploited to provided improved
tolerance to environmental stresses and conserved BCA capacity.
Alternatives to synthetic pesticides and biological control agents produced
commercially are being sought in many areas of plant production. Compost teas are being
extensively used in urban, horticultural and agriculture settings for their fertility and disease
x