Microbiology

Conspirators in blight

A fungus and a bacterium have been found in a symbiotic alliance that attacks rice plants. Rice feeds more people than any other crop, but the significance of this finding extends beyond its potential agricultural use.

Rice suffers from a serious disease called seedling blight. The cause was thought to be a toxin released by some species of the fungal group Rhizopus. The toxin kills root cells, after which the fungus digests the remains of the dead root. But as Partida-Martinez and Hertweck report on page 884 of this issue1, that is not the case — they find that the toxin is produced not by the fungus, but by bacteria that live in symbiosis inside it.

This finding may help in controlling seedling blight, no minor consideration given that rice feeds more people in the world than any other crop plant (Fig. 1). Moreover, the toxin — rhizoxin — stops cell division in some lines of human cancer cells. It is under investigation as a potential antitumour agent, so identification of the genes involved in rhizoxin production could also provide lessons for cancer researchers.

Figure 1: Rice under cultivation in Vietnam.
figure1

P. BRONSTEIN/GETTY

World production in 2004 exceeded 600 million tonnes7, but rice plants are prey to many diseases, including seedling blight.

An enzyme, a polyketide synthase (PKS), has been implicated in the biosynthesis of rhizoxin, which is associated with only some species, or strains, of Rhizopus. But when Partida-Martinez and Hertweck looked for fungal PKS genes in the genome of Rhizopus strains known to release the toxin, they could not find them. However, the authors did detect PKS genes in the fungus that were similar to a known class of bacterial PKS genes.

The next and obvious question was whether these genes really exist in bacteria living inside the fungus. Partida-Martinez and Hertweck first amplified and sequenced a particular set of genes — 16S ribosomal genes, unique to bacteria — from DNA extracted from the fungus (which would include DNA of any bacteria living inside it). They found that the 16S sequences belong to bacteria of the genus Burkholderia, a group that occupies a remarkably wide range of ecological niches2. Burkholderia 16S genes were not found in strains of Rhizopus that do not release the toxin.

Using laser microscopy, the authors were able to observe bacteria living inside toxin-producing Rhizopus strains. They then treated these strains with antibiotics and showed, again with laser microscopy, that the fungus no longer contained the bacteria. Bacterial genes were not evident in these bacterium-free strains, and the fungus did not release detectable amounts of rhizoxin.

From these findings, it seemed likely that Burkholderia bacteria were producing the toxin that causes rice seedling blight. But Partida-Martinez and Hertweck went further. Bacteria that live inside other organisms are notoriously difficult to culture on artificial media, and many are considered unculturable3. However, Partida-Martinez and Hertweck successfully isolated the bacteria and cultured them without their fungal host. They showed that it was indeed a pure culture of a species of Burkholderia and that it produced the toxin in artificial media. When the bac-teria were reintroduced into a bacterium-free fungus, the fungus again produced significant amounts of rhizoxin. Although the toxin stops cell division in human cells, for example, it clearly doesn't harm the fungus.

The exciting aspects of this research1 go beyond the prospects for controlling seedling blight in rice and using rhizoxin to treat cancer: the existence and evolution of such a symbiosis between the fungus and bacterium are in themselves intriguing. Close relatives of Burkholderia are well known as symbionts that commonly live inside other fungi, called arbuscular mycorrhizal fungi, which in turn live symbiotically in the roots of most plant species4,5. The role of these bacteria in mycorrhizal fungi has remained elusive because of the difficulty of culturing them. So the new work also tells us more about a Burkholderia–fungus association.

Finally, Partida-Martinez and Hertweck found that although bacterial production of rhizoxin occurs outside the host, it diminishes over time. This may, however, simply be a consequence of an artificial medium that was not entirely favourable to bacterial growth, and does not necessarily mean that the bacteria cannot sustain toxin production in the absence of a host. Burkholderia bacteria are known to cause disease in plants2, but the fact that they do so in a symbiosis with a fungus is a new finding.

So what's in it for the partners? At this stage, we can only speculate, but there could be several benefits for the bacteria. For example, the fungus may act as a vector for rapid bacterial dispersal to new roots. Further, much plant tissue is difficult to degrade, but fungi are particularly well equipped with the enzymes to do this; presumably, the bacteria reap the benefits of their toxin production when the fungus digests the dead plant cells. For the fungus, toxin release results in a supply of dead organic matter to digest and perhaps also deters other competitors.

More than 125 years ago, biological symbiosis was first defined by Anton de Bary as simply the cohabitation of two different organisms6. Since then it has gradually become clear that the spectrum of relationships varies from beneficial mutualism to outright parasitism. Partida-Martinez and Hertweck's work adds a fresh aspect to our understanding of such relationships — that the apparently beneficial existence of two organisms can occur at the expense of a third one.

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Sanders, I. Conspirators in blight. Nature 437, 823–824 (2005). https://doi.org/10.1038/437823a

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