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Beneficial microorganisms for sustainable agriculture

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OFFICIAL JOURNAL OF THE AUSTRALIAN SOCIETY FOR MICROBIOLOGY INC.
Volume 33 Number 3 September 2012

Microorganisms:
Their benefits and beyond

Beneficial microorganisms for sustainable
agriculture
Vadakattu V.S.R. Gupta
Vadakattu V.S.R. Gupta
CSIRO Ecosystem Sciences
PMB 2, Glen Osmond, SA 5064
Australia
Tel +61 8 8303 8579
Email gupta.vadukattu@csiro.au
Global agriculture has to double food production by 2050
in order to feed the world’s growing population and at
the same time reduce its reliance on inorganic fertilisers
and pesticides. To achieve this goal, there is an urgent
need to harness the multiple beneficial interactions
that occur between plants and microorganisms. The
beneficial influences of microorganisms on plant growth
include nitrogen fixation, acquisition and uptake of
major nutrients, promotion of shoot and root growth,
disease control or suppression and improved soil
structure. Some of the commonly promoted and used
beneficial microorganisms in agriculture worldwide
include Rhizobia, Mycorrhizae, Azospirillum, Bacillus,
Pseudomonas, Trichoderma, Streptomyces species and
many more. Unravelling the biota black box using
modern molecular methods is helping to find new suites
of beneficial microorganisms that can help improve
agricultural production worldwide.
N2 fixing bacteria
Symbiotic associations between legume plants and root-
nodulating bacteria belonging to the genera Rhizobium,
Bradyrhizobium, Ensifer and Mesorhizobium produce around
80% of the nitrogen in Australian grains, with a value estimated
at A$3 billion each year1. Nitrogen fixation is one of the
essential beneficial biological processes for the economic and
environmental sustainability of agriculture worldwide. Globally,
annual inputs of fixed nitrogen from crop legume–rhizobia
symbioses are estimated as 2.95 million tonnes for pulses and
18.5 million tonnes for oilseed legumes1. In spite of the in-depth
knowledge about the biochemical and molecular steps involved
in legume-rhizobium symbiosis, the holy grail of N2 fixation by
non-legumes, especially cereal food crops, is yet to be realised.
Finding efficient rhizobia for the wide variety of legumes
that are cultivated around the world and developing efficient
management of symbioses in the field to realise the ~25 kg of
M I CROB I O L O G Y A U S T RALIA • SE P T E MB E R 2 0 1 2 
Under the Microscope
N2 fixation for each tonne of legume dry matter are the major
challenges for the future.
"Diazotrophy", the ability to fix atmospheric nitrogen catalysed by
the enzyme nitrogenase, is distributed among diverse groups of
bacteria and archaea2. Free-living N2 fixing bacteria (for example,
Azospirillum spp., Azotobacter spp., Acetobacter diazotrophicus,
Herbaspirillum spp., Bacillus spp., Azoarcus sp.) are found in
the rhizosphere and rhizoplane environments of cereal crops.
Recent evidence not only identified new genera of N2 fixing
bacteria and archaea in natural and managed ecosystems but
also indicated significant edaphic and environmental groupings
in genetic diversity and functionality3,4. Non-rhizobial N2 fixing
bacteria can grow as endophytes in a number of grasses, for
example, in a recent study in South Australia Pseudomonas
species were the most dominant group of nifH carrying bacteria
found in the rhizosphere of perennial native grasses5. Evidence
suggests the nifH gene is present in a number of non-Frankia
actinobacteria (for example, Agromyces, Microbacterium,
Corynebacterium and Micromonospora).
Thus the challenge is to identify (i) functionally significant N2
fixing genera/species specific to biomes and crops, and (ii)
key edaphic and environmental drivers regulating the genetic
diversity and free living N2 fixation in order to maximise benefits
from these beneficial microbes both for sustainable primary
production and climate change adaptation.
Mycorrhizae and phosphate solubilising
microorganisms
The symbiotic association of plants and mycorrhizal fungi
(arbuscular mycorrhizal fungi, AMF) has long been recognised
for the benefits it provides with nutrient transport and uptake;
however, there is considerable uncertainty about the functional
benefits in intensive agricultural systems5,6. Even though AM
symbiosis is widespread, the symbiotic functions of AMF species
differ according to specific AMF isolates, host plants and soil
properties. AMF associations are generally considered diffuse
and non-specific because multiple species colonisation linking
together two or more plants is not uncommon7. Identification
of specific phylotypes of AMF and their relationship with
soil properties is a crucial step to fully exploit the benefits
from AMF6,7. New knowledge on the microbial interactions in
the mycosphere has the potential to enhance our ability to
manipulate plant-mycorrhizal associations. Restoration of AMF
symbiosis is one of the key beneficial biological processes for the
rehabilitation of contaminated soils and mining sites6.
113
Under the Microscope
A diverse array of bacteria (for example, Pseudomonas, Bacillus,
actinomycetes) and fungi (for example, Aspergillus, Penicillium
species) are capable of solubilising and mineralising plant
unavailable forms of phosphorus in soils, and the benefits
from their use as inoculants are increasingly being recognised,
especially in P-limited environments8,9.
Plant growth-promoting rhizobacteria (PGPR)
Bacteria colonising roots that elicit shoot and root growth,
referred generally as PGPR, are recommended (marketed) for
improving plant growth and disease control both in agriculture
and horticulture10. PGPR can promote root and shoot growth
either by producing plant hormones or secondary metabolites,
controlling diseases, induction of systemic resistance or through
changing physicochemical interactions with plants. Bacterial
inoculants applied as bio-fertilisers are also being explored to
alleviate stress from abiotic factors, for example, drought and
salinity11.
Biological control organisms
Bacteria, fungi and actinobacteria can act as biocontrol agents
against root diseases12. A number of bacterial and fungal inoculant
formulations are available commercially to control diseases
in agricultural and horticultural crops (http://www.oardc.ohio-
state.edu/apsbcc/). Challenges associated with the introduction
of biocontrol organisms against soil-borne plant pathogens
include their poor survival, variable root colonisation and lack
of adaptability to the natural environment. The success of
biocontrol inoculants depends upon the ability to: (1) maintain
the adequate populations needed to provide effective biological
control; (2) lengthen the period during which a threshold
population density is sustained in the rhizosphere; and (3)
increase the magnitude of disease control provided by introduced
rhizobacteria. Actinobacterial endophytes can colonise plants
without disrupting the "normal" endophytic populations, can
produce antifungal antibiotics and plant growth hormones, and
can also induce systemic disease resistance in plants13. Biocontrol
Figure 1. Natural biological suppression can reduce the impact of rhizoctonia disease in cereal crops. Inset: Damaged hyphae of Rhizoctonia
solani AG8 in a suppressive soil.
Footnote: Enhanced biological disease suppression mediated by a variety of bacteria, actinomycetes and fungi has been identified under
conservation management practices in South Australia. Unravelling the composition of such microbial communities has the potential to identify
a new suite of beneficial microbes.
114
inoculants are generally tested for their antibiosis potential due
to antagonism, hyper-parasitism, competition and predation
by indigenous organisms; however, organisms that induce a
systemic resistance to diseases and pests have the greatest
potential to succeed under field conditions10.
Some soils can suppress the severity of disease even in the
presence of a pathogen, host plant and favourable climatic
conditions for the disease. There are a number of examples,
both in Australia (Figure 1) and worldwide, where agricultural
soils have become suppressive to soil-borne pathogens14-16.
Culture-based and culture-independent analyses have indicated
the involvement of a diverse range of microorganisms involved
in reducing pathogen inoculum and infection, plant growth
promotion and induction systemic resistance (Table 1). Due to
the difficulties associated with introducing inoculants, in situ
enhancement of beneficial microorganisms involved in natural
disease suppression could be the more effective and reliable
control measure. It can also provide environmental benefits by
reducing agrochemical dependency for disease control.
Probiotics for plants
Probiotics for human health are not new but the concept of
managing plant health through the manipulation of probiotic
organisms associated with plants has gained interest only
recently17. Plant-specific stimulation of specific microbial groups
in their rhizosphere suggests that plants may have evolved to
strategically stimulate and support particular microbial groups
capable of producing antibiotics as a defence against diseases
caused by soil-borne pathogens16. Diseases caused by soil-borne
fungal pathogens result in more than $150 million of annual
production losses in cereal crops in Australia.
Soil bacteria belonging to the genus Pseudomonas are ubiquitous
in most soils and have been linked to wide-ranging processes
including plant growth promotion and inhibition, disease
control, nutrient cycling, nitrogen fixation and bioremediation.
MICROBIOLOG Y A U STRA LIA • SEPTEM BER 2012

Their ability to respond quickly to changes in physical, chemical,
carbon and nutritional conditions in soil has been linked to their
functional significance in agricultural ecosystems. Pseudomonads
have been studied for their biocontrol potential against fungi and
oomycete pathogens for more than two decades and a number of
promising candidates have been identified18. Antibiosis is the most
commonly suggested trait responsible for their activity against
plant pathogens and a number of antimicrobial compounds
have been identified, for example, 2,4-diacetylphloroglucinol
(2,4-DAPG), phenazines (PHZ), pyrrolnitrin (PRN), pyoluteorin
(PLT), hydrogen cyanide (HCN) and biosurfactant antibiotics17.
Conventional biochemistry-based characterisation of the
chemicals is now complemented with molecular techniques (e.g.
metabolomics and transcriptomics) to unravel the mechanisms
of production, interactions with pathogens and plants, genotypic
and phenotypic diversity of organisms capable of producing
similar compounds and determine their activity in natural soil
environments.
Finding new beneficial inoculants
Traditional cultivation and isolation methods have mainly targeted
a small group of copiotrophic microorganisms as candidates for
inoculants. Culture-independent investigations have revealed the
presence of significant populations of new bacterial divisions (for
example, Verrucomicrobia, Acidobacteria) in the rhizosphere
which were not identified in the isolations using nutrient-rich
media. Pyrosequencing targeting the surface protein encoding
cpn60 could help generate a list of genera and their relative
abundances in situ, which can complement the isolation efforts
using semi-selective culture media and specialised cultivation
methods19,20.
Table 1. List of beneficial organisms isolated from suppressive soil
}
with demonstrated functions in the suppression of diseases caused
by soilborne necrotrophic pathogens15.
Organisms Functions
Bacillus spp. Reduced pathogen inoculum
Microbacteria spp. Competition
Pseudomonas brassicacearum Parasitism
Pantoea agglomerans Predation
Exiguobacterium acetylicum Reduced infection
Pseudomonas fluorescens General antibiosis
Streptoverticillium sp. Disrupt growth of pathogen from
source to root
Streptomyces spp. Prevent access to infection sites
Trichoderma spp. Metabolise/disrupt plant-microbe
signalling
Penicillium griseofulvum General antibiosis
Mycophagous amoebae Induced systemic resistance
Fungal feeding nematodes Plant growth promotion
Production of secondary roots
Improved nutrient availability
M I CROB I O L O G Y A U S T RALIA • SE P T E MB E R 2 0 1 2 
Under the Microscope
Conclusion
It is essential to enhance the activities of microbes that benefit plant
nutrition, control diseases and assist plants to cope with a variety
of abiotic stresses to sustain and improve global food production
in future climate scenarios while maintaining environmental
health. A diverse range of beneficial microorganisms have been
found but their reliable use in field environments is yet to be fully
realised. New knowledge on soil microbial diversity can lead to
the discovery of new generation inoculants as well as improve
survival and performance of beneficial microbes in situ following
their introduction into foreign environments.
Acknowledgements
The author wishes to acknowledge the CSIRO Ecosystem
Sciences and Grains RDC for financial support (CSP00135)
and present and past colleagues for the numerous helpful
discussions.
References
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agriculture – Foreword. Aust. J. Exp. Agric. 45, ii.
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contemporary perspective. Annu. Rev. Ecol. Evol. Syst. 42, 489–512.
3. Buckley, D.H. et al. (2007) Stable isotope probing with 15N2 reveals novel
non-cultivated diazotrophs in soil. Appl. Environ. Microbiol. 73, 3196–3204.
4. Wakelin, S.A. et al. (2011) Regional and local factors affecting diversity,
abundance and activity of free-living N2-fixing bacteria in Australian agricultural
soils. Pedobiologia. 53, 391–399.
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conference 25–30 September 2011, Perth, Australia.
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Biography
Dr. Vadakattu Gupta is a principal research scientist in CSIRO
Ecosystem Sciences at Waite campus in Adelaide. His research
interests are in the areas of functional microbial ecology and
plant-microbe-soil interactions with current focus on unravelling
the genetic and functional diversity of disease suppressive
microbial communities and rhizosphere dynamics of microbiota
and biological functions.
115
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