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NODULE BACTERIA: CAN THEY BE CONSIDERED AN AGENT OF DISEASE?
J.G. Howieson A , M. Gerding and G.W. O’Hara A
A : Centre for Rhizobium Studies
Murdoch University, Murdoch WA 6150
ABSTRACT. Nodule bacteria from the alpha and beta proteobacterial classes can invade the roots of legumes. On many
occasions, the outcome of this invasion is the formation of a functional nodule able to house the bacteria in such a way that
the nitrogenase enzyme can “fix” atmospheric dinitrogen into plant available forms. However, not infrequently the
relationship is dysfunctional, the association does not lead to nitrogen fixation, and the bacteria can be considered more an
agent of disease than a symbiont. This paper reveals two ways in which nodule bacteria can be a hindrance to legume
development and productivity, rather than an asset. The first example is that of the transfer of a symbiosis island from an
inoculant in the genus Mesorhizobium to soil-borne bacteria previously unable to nodulate. The second is where exotic
legumes introduced to Australia are nodulated by the nodule bacteria already in our soils, to the exclusion of more
appropriate inoculant strains. In both scenarios, ineffective nodulation resulted, and the legume was unable to prosper, taking
on the manifestation of a diseased plant.
INTRODUCTION
The legumes and their nodule bacteria exploited in
Australian agriculture are almost entirely exotic to this
continent, having their origins primarily in Mediterranean
Europe, South America and Africa. The process of
improving legume performance is ongoing, through
development of new legumes for commerce, and strains of
rhizobia that are more effective at nitrogen fixation. In both
cases this requires introducing new genetic material to
Australian soils, and this material has the potential to
interact with the existing biota in different ways. In pursuing
legume improvement, we have encountered obstacles to
optimising symbiosis, and this manuscript describes two
examples of such obstacles that have emerged in the last 15
years.
We are currently searching the globe for robust types of
perennial legume that might be suitable for domestication as
plants adapted to a changing climate in WA. Lessertia is a
legume genus common in the fynbos flora of the Western
Cape of South Africa. The genus has over 50 species,
several of which are herbaceous, perennial forages (e.g. L
capitata, L. herbacea and L hirsuta). We have attempted to
domesticate these species however field experiments with
them failed to establish because of issues of nodulation.
In a similar but more successful vein, Biserrula pelecinus
was domesticated in WA in the early 1990s and then
introduced to faming as an acid tolerant legume adapted to
infertile soils (Howieson et al 1995). Its microsymbiont,
Mesorhizobium ciceri bv biserrulae was also introduced to
this environment. We have undertaken studies of the fate of
this microsymbiont, following its widespread use as an
inoculant.
MATERIALS AND METHODS
Lessertia Root nodules from species of Lessertia were
collected from a wide range of sites in the Western Cape
region of South Africa (Gerding et al 2012). Seeds were also
collected where possible. In Perth, 43 isolates from the
Lessertia nodules were authenticated then stored in the
WSM culture collection at the Centre for Rhizobium
Studies, Murdoch University. Effective strains were
prepared as inoculants for field experiments. Seeds were
multiplied in the plots and glasshouses at Murdoch
University.
Biserrula Biserrula was commercialised in 1997, with
inoculant strains made available to manufacturers. Fields
sown prior to 2000 were visited several years later, nodules
collected from plants that had regenerated, and the
occupants of these nodules identified.
RESULTS
Lessertia The species of nodule bacteria isolated from
Lessertia nodules collected in South Africa were dominantly
of the genus Mesorhizobium (Gerding et al 2012). Plants
inoculated with some of these strains selected for high N
fixation failed to thrive in six field experiments in WA.
Growth was poor and plants were yellow and unthrifty, with
root systems containing small and white nodules. When
nodules were harvested from surviving Lessertia plants, the
nodule occupants were typed by RAPD PCR and found to
be of the genus Rhizobium. Attempts were made in
subsequent experiments to hyper-inoculate Lessertia with
compatible strains of mesorhizobia, however nodule
occupancy was dominantly by Rhizobium and plants failed
to thrive (Macarena Gerding 2012 PhD Thesis, Murdoch
University).
Biserrula A small number of nodules on the roots of
regenerating biserrula stands were small and white. Analysis
of the organisms inside these nodules showed them to be
species other than the inoculant strains. In fact, two
previously undescribed species of Mesorhizobium were
found in these nodules: M. australiticum and M.
opportunistum (Nandasena et al 2009). Unfortunately, these
species were unable to fix nitrogen when inside the biserrula
nodules. Further study showed these new rhizobial species
contained symbiotic DNA from the original inoculant strains
in the form of a “symbiosis island” that transferred from the
original inoculant to resident bacteria in the soil. The high
level of adaptation of these resident bacteria to the soil
conditions allowed them to outcompete inoculant strains for
nodulation of biserrula plants.
DISCUSSION
In both the situations described, nodule bacteria other than
the desired inoculants were able to nodulate the pasture
legumes under development. In the case of Lessertia, this
competition was so severe that it became clear that Lessertia
could not be continued in its development for agriculture. In
the case of biserrula, the emerging nodulating species have
so far not overwhelmingly compromised production.
However, in both scenarios, the nodule bacteria responsible
for the ineffective nodulation could be described as agents
of disease.
REFERENCES
1. Howieson, J. G., Loi, A. and Carr, S. J. (1995).
Australian Journal of Agricultural Research 46:997–
1007.
2. Nandasena, K., O’Hara G.W., Tiwari, R., Willems, A.
and Howieson J.G. (2009) International Journal of
Systematic and Evolutionary Microbiology (2009), 59,
2140–2147.
3. Gerding M., O’Hara, G.W., Bräu, L, Nandasena, K. and
Howieson, J.G. (2012) Plant and Soil DOI
10.1007/s11104-012-1153-3.
7th Australasian Soilborne Diseases Symposium 6