Associative and Endophytic Nitrogen-fixing Bacteria and Cyanobacterial Associations

336 Pages·2007·5.387 MB·English

by  C. Elmerich (auth.), Claudine Elmerich, William E. Newton (eds.)

Associative and Endophytic Nitrogen-fixing Bacteria
and Cyanobacterial Associations
NitrogenFixation:Origins,Applications,andResearchProgress
VOLUME 5
Thetitlespublishedinthisseriesarelistedattheendofthisvolume.
Associative
and Endophytic
Nitrogen-fixing Bacteria
and Cyanobacterial
Associations
Edited by
Claudine Elmerich
InstitutPasteur,
Paris,France
and
William E. Newton
DepartmentofBiochemistry
VirginiaPolytechnicInstituteandStateUniversity
Blacksburg,Virginia,U.S.A.
AC.I.P.CataloguerecordforthisbookisavailablefromtheLibraryofCongress.
ISBN-101-4020-3541-1(HB)
ISBN-13978-1-4020-3541-8(HB)
ISBN-101-4020-3546-2(e-book)
ISBN-13978-1-4020-3546-3(e-book)
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TABLE OF CONTENTS
Preface to the Series. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix
Preface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii
List of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xvii
Dedication – Johanna Döbereiner . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . xxi
Chapter 1. Historical Perspective: From Bacterization to Endophytes
C. Elmerich . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1. The Nitrogen Cycle: Heritage from the 19th Century . . . . . . . . . . . . . 1
2. Nutritional Interactions between Bacteria and Plants . . . . . . . . . . . . . 3
3. Associative Nitrogen-fixing Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . 8
4. Discovery of Nitrogen-fixing Endophytes . . . . . . . . . . . . . . . . . . . . 11
5. Cyanobacterial Associations . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . 14
6. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

Chapter 2. Molecular Phylogeny and Ecology of Root Associated
Diazotrophic (cid:302)- and (cid:533)-Proteobacteria
M. Schmid and A. Hartmann . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
2. Tools for Molecular Phylogeny and in situ Localization
of Bacterial Isolates and Communities . . . . . . . . . . . . . . . . . . . . . 23
3. Molecular Phylogeny and Ecology of Azospirillum and Other
Nitrogen-fixing (cid:302)-Subclass Proteobacteria . . . . . . . . . . . . . . . . . . . 27
4. Molecular Phylogeny and Ecology of Herbaspirillum, Diazotrophic
Burkholderia spp., and Other N -fixing (cid:533)-Proteobacteria . . . 29
2
5. Conclusions and Prospects for Future Studies. . . . . . . . . . . . . . . . . . 35
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
Chapter 3. Regulation of Nitrogen Fixation and Ammonium Assimilation
in Associative and Endophytic Nitrogen fixing Bacteria
F. O. Pedrosa and C. Elmerich . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
2. Rhizospheric and Endophytic Bacteria: General Features . . . . . . . . 42
3. Structural Organization of nif Genes . . . . . . . . . . . . . . . . . . . . . . . . 44
4. Identification of RpoN and Its Involvement in Nitrogen Fixation . . 48
5. The Ntr System and the Control of Nitrogen Metabolism
and Nitrogen Fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49
6. Regulation of Nitrogen Fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
v
vi TABLEOFCONTENTS
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
Chapter 4. Chemotaxis in Soil Diazotrophs: Survival and Adaptative Response
G. Alexandre and I. B. Zhulin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
2. Gene-Expression Regulation and Chemotaxis as Adaptive
Responses to Environmental Changes . . . . . . . . . . . . . . . . . . . . . 74
3. Molecular Mechanism of the Chemotactic Response: Learning
from Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
4. Directed Motility in Soil Diazotrophs . . . . . . . . . . . . . . . . . . . . . . . 78
5. Future Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
Chapter 5. Molecular Genetics of Rhizosphere and Plant-Root Colonization
E. Vanbleu and J. Vanderleyden . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
2. Motility of Associative Diazotrophs . . . . . . . . . . . . . . . . . . . . . . . . 86
3. Attachment to Plant Roots . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
4. Rhizosphere Competence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Chapter 6. Microbial Production of Plant Hormones
B. E. Baca and C. Elmerich . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113
1. Discovery of Phytohormones . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113
2. Production and Role of Phytohormones . . . . . . . . . . . . . . . . . . . . . 115
3. Pathways for Plant Hormone Biosynthesis: Common Routes
in Plants, Bacteria and Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
4. Major Routes for IAA synthesis in Pathogenic and Beneficial
Nitrogen-fixing Bacteria Associated with Plants . . . . . . . . . . . . 123
5. Multiple Routes for IAA Synthesis in Azospirillum . . . . . . . . . . . . 127
6. Other Phytohormones Produced by Plant Pathogenic and
Nitrogen-fixing Associated and Endophytic Bacteria . . . . . . . . . 130
7. Plant Growth Promotion (PGP): Role of Bacterial Phytohormone
Production, ACC-Deaminase, and Use of Synthetic Auxins . 133
8. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137
Chapter 7. The Plant Growth-Promoting Effect and Plant Responses
S. Dobbelaere and Y. Okon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145
1. N Fixation vs. “Hormonal” Effects: Historical Perspectives . . . . . 145
2
2. Effects of Azospirillum and Other Diazotrophs
on Root Morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
TABLEOFCONTENTS vii
3. Effects on Root Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 154
4. Effects on Plant Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
5. Future Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164
Chapter 8. Biocontrol of Plant Diseases by Associative and Endophytic
Nitrogen-fixing Bacteria
R. Bally and C. Elmerich . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171
1. Beneficial Plant-Associated Nitrogen-fixing Bacteria and
Biocontrol of Plant Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171
2. Interactions within Microbial Communities: Competition
Mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 172
3. Biological Control against Soil-Borne Diseases . . . . . . . . . . . . . . . 174
4. Regulation of Biocontrol Properties and Cell-Cell
Communication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
5. Plant Response to Pathogens and Biological Control
in the Rhizosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 182
6. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184
Chapter 9. Endophytic Associations of Azoarcus spp.
B. Reinhold-Hurek and T. Hurek . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 191
2. The Rise of Interest in Diazotrophic Endophytes . . . . . . . . . . . . . . 192
3. Azoarcus spp. and related Genera: Strictly Plant-Associated
versus Soil Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 194
4. Habitats and Ecophysiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 198
5. Interactions with Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201
6. Infection of Roots by Endophytic Diazotrophs: An Active,
Specific Process? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202
7. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207
Chapter 10. Biological Nitrogen Fixation in Sugarcane
V. Reis, S. Lee and C. Kennedy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213
1. Short Story of the Sugarcane-Cropping System . . . . . . . . . . . . . 213
2. Nitrogen-fixing Bacteria Colonising Sugarcane: New
Phylogenetic Data, Properties, and Endophytic Status . . . . . . . . 215
3. Contribution of BNF to the Sugarcane Crop . . . . . . . . . . . . . . . . . . 219
4. Effect of N Fertilization on BNF . . . . . . . . . . . . . . . . . . . . . . . . . . . 220
5. Genes for Nitrogen Fixation and Their Regulation in
G. diazotrophicus and H. seropedicae . . . . . . . . . . . . . . . . . . . . . 221
6. Is Indole Acetic Acid Production an Important Factor in the Ability
of G. diazotrophicus to Enhance Growth of Sugarcane? . . . . . . . 225
7. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 226
viii TABLEOFCONTENTS
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 228
Chapter 11. Heterocyst Differentiation and Nitrogen Fixation in Cyanobacteria
R. Haselkorn . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233
1. Early History of the Association of Nitrogen Fixation
with Heterocysts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 233
2. Cyanobacterial Nitrogenase and nif-Genes Organization . . . . . . . . 236
3. Pathway of N Assimilation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239
4. Carbon Metabolism in Heterocysts . . . . . . . . . . . . . . . . . . . . . . . . . 240
5. Genetic Tools for Studying Cyanobacterial Nitrogen Fixation . . . . 241
6. Regulatory Genes Required for Heterocyst Differentiation . . . . . . . 242
7. Prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252
Chapter 12. Cyanobacterial Associations
B. Bergman, A. N. Rai, and U. Rasmussen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
2. Historical Aspects and Landmarks . . . . . . . . . . . . . . . . . . . . . . . . . 259
3. Symbioses with Diatoms (Algae) . . . . . . . . . . . . . . . . . . . . . . . . . . 261
4. Symbioses with Fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264
5. Symbiosis with Bryophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 270
6. Symbiosis with Pteridophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274
7. Symbioses with Cycads . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277
8. Symbiosis with Gunnera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 282
9. Creation of New Symbioses and Prospects . . . . . . . . . . . . . . . . . . . 290
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292
Chapter 13. Prospects for Significant Nitrogen Fixation in Grasses
from Bacterial Endophytes
E. W. Triplett . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303
1. Ultimate Objective of Nitrogen-fixation Research – Nitrogen
Fixation in Maize, Wheat, and Rice . . . . . . . . . . . . . . . . . . . . . . 303
2. Understanding the Basic Biology of Endophytic Colonization: Using
Klebsiella pneumoniae 342 (Kp342) as the Model Diazotrophic
Endophyte. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . 305
3. Attributes Needed for a Model Diazotrophic Endophyte . . . . . . . . 307
4. Future Work Needed to Replace Nitrogen Fertilizer with
Diazotrophic Endophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 310
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 312
Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315
PREFACE TO THE SERIES
Nitrogen Fixation: Origins, Applications, and Research Progress
Nitrogen fixation, along with photosynthesis as the energy supplier, is the basis of
all life on Earth (and maybe elsewhere too!). Nitrogen fixation provides the basic
component, fixed nitrogen as ammonia, of two major groups of macromolecules,
namely nucleic acids and proteins. Fixed nitrogen is required for the N-containing
heterocycles (or bases) that constitute the essential coding entities of
deoxyribonucleic acids (DNA) and ribonucleic acids (RNA), which are responsible
for the high-fidelity storage and transfer of genetic information, respectively. It is
also required for the amino-acid residues of the proteins, which are encoded by the
DNA and that actually do the work in living cells. At the turn of the millennium, it
seemed to me that now was as good a time as any (and maybe better than most) to
look back, particularly over the last 100 years or so, and ponder just what had been
achieved. What is the state of our knowledge of nitrogen fixation, both biological
and abiological? How has this knowledge been used and what are its impacts on
humanity?
In an attempt to answer these questions and to capture the essence of our
current knowledge, I devised a seven-volume series, which was designed to cover
all aspects of nitrogen-fixation research. I then approached my long-time contact at
Kluwer Academic Publishers, Ad Plaizier, with the idea. I had worked with Ad for
many years on the publication of the Proceedings of most of the International
Congresses on Nitrogen Fixation. My personal belief is that congresses, symposia,
and workshops must not be closed shops and that those of us unable to attend
should have access to the material presented. My solution is to capture the material
in print in the form of proceedings. So it was quite natural for me to turn to the
printed word for this detailed review of nitrogen fixation. Ad’s immediate
affirmation of the project encouraged me to share my initial design with many of
my current co-editors and, with their assistance, to develop the detailed contents of
each of the seven volumes and to enlist prospective authors for each chapter.
There are many ways in which the subject matter could be divided. Our
decision was to break it down as follows: nitrogenases, commercial processes, and
relevant chemical models; genetics and regulation; genomes and genomics;
associative, endophytic, and cyanobacterial systems; actinorhizal associations;
leguminous symbioses; and agriculture, forestry, ecology, and the environment. I
feel very fortunate to have been able to recruit some outstanding researchers as co-
editors for this project. My co-editors were Mike Dilworth, Claudine Elmerich,
John Gallon, Euan James, Werner Klipp, Bernd Masepohl, Rafael Palacios,
Katharina Pawlowski, Ray Richards, Barry Smith, Janet Sprent, and Dietrich
Werner. They worked very hard and ably and were most willing to keep the
volumes moving along reasonably close to our initial timetable. All have been a
pleasure to work with and I thank them all for their support and unflagging interest.
ix
x PREFACE TOTHE SERIES
Nitrogen-fixation research and its application to agriculture have been ongoing
for many centuries – from even before it was recognized as nitrogen fixation. The
Romans developed the crop-rotation system over 2000 years ago for maintaining
and improving soil fertility with nitrogen-fixing legumes as an integral component.
Even though crop rotation and the use of legumes was practiced widely but
intermittently since then, it wasn’t until 1800 years later that insight came as to how
legumes produced their beneficial effect. Now, we know that bacteria are harbored
within nodules on the legumes’ roots and that they are responsible for fixing N and
2
providing these plants with much of the fixed nitrogen required for healthy growth.
Because some of the fixed nitrogen remains in the unharvested parts of the crop, its
release to the soil by mineralization of the residue explains the follow-up beneficial
impact of legumes. With this realization, and over the next 100 years or so,
commercial inoculants, which ensured successful bacterial nodulation of legume
crops, became available. Then, in the early 1900’s, abiological sources of fixed
nitrogen were developed, most notable of these was the Haber-Bosch process.
Because fixed nitrogen is almost always the limiting nutrient in agriculture, the
resulting massive increase in synthetic fixed-nitrogen available for fertilizer has
enabled the enormous increase in food production over the second half of the 20th
century, particularly when coupled with the new “green revolution” crop varieties.
Never before in human history has the global population enjoyed such a substantial
supply of food.
Unfortunately, this bright shiny coin has a slightly tarnished side! The
abundance of nitrogen fertilizer has removed the necessity to plant forage legumes
and to return animal manures to fields to replenish their fertility. The result is a
continuing loss of soil organic matter, which decreases the soil’s tilth, its water-
holding capacity, and its ability to support microbial populations. Nowadays, farms
do not operate as self-contained recycling units for crop nutrients; fertilizers are
trucked in and meat and food crops are trucked out. And if it’s not recycled, how
do we dispose of all of the animal waste, which is rich in fixed nitrogen, coming
from feedlots, broiler houses, and pig farms? And what is the environmental impact
of its disposal? This problem is compounded by inappropriate agricultural practice
in many countries, where the plentiful supply of cheap commercial nitrogen
fertilizer, plus farm subsidies, has encouraged high (and increasing) application
rates. In these circumstances, only about half (at best) of the applied nitrogen
reaches the crop plant for which it was intended; the rest leaches and “runs off” into
streams, rivers, lakes, and finally into coastal waters. The resulting eutrophication
can be detrimental to marine life. If it encroaches on drinking-water supplies, a
human health hazard is possible. Furthermore, oxidation of urea and ammonium
fertilizers to nitrate progressively acidifies the soil – a major problem in many
agricultural areas of the world. A related problem is the emission of nitrogen oxides
(NO ) from the soil by the action of microorganisms on the applied fertilizer and, if
x
fertilizer is surface broadcast, a large proportion may be volatilized and lost as
ammonia. For urea in rice paddies, an extreme example, as much as 50% is
volatilized and lost to the atmosphere. And what goes up must come down; in the
case of fertilizer nitrogen, it returns to Earth in the rain, often acidic in nature. This