As one of the three toxic metal elements and the ten cancerogenic chemicals, mercury is a notorious environmental toxin and health killer. Prof. FANG Weiguo at the Zhejiang University College of Life Sciences identified two genes in the plant symbiotic fungus Metarhizium robertsii. They could convert the neurotoxin methylmercury (MeHg) into divalent mercury (Hg2+), which could be further reduced to the volatile elemental mercury (Hg0). Not only does this mechanism enable M. robertsii to "detoxify the toxin for itself", but it also provides a natural defense against the threat of mercury to the its symbiotic partner plants. This intriguing discovery came out in PNAS on November 15.
M. robertsii resembles a patch of Penicillium fungi that grow on the skin of a putrefying tangerine, with dark green spores lurking beneath white mycelia. In agriculture, it is an extensively used biological pesticide. If you see the "moldy" dried bodies of green insects, chances are that they are decimated by M. robertsii. This fungus can effectively infect many pests, such as locusts, moths and mosquitoes in the field, grow and flourish on their host, and eventually make their host "green" and "stiff".
Locusts infected with Metarhizium robertsii
However, such a deadly fungus is a gentle guardian of plants. M. robertsii thrives in the root system of plants, dissolving phosphorus in the soil for better absorption by plants, which "give back" the glucose they make to M. robertsii. Meanwhile, it helps plants to defend themselves against some microbial pathogens. This mutually beneficial relationship has been in existence for millions of years on Earth.
Prof. Fang has been long fascinated by the "gentle" and "ferocious" M. robertsii. In his eyes, its 11,000 genes are a giant treasure trove, and each gene is worth investigating. "We endeavor to decipher the mechanisms behind the interesting traits from a genetic and evolution point of view. One of them is the genetic evolutionary mechanism in regard to which gene leads to its macroscopic idiosyncrasy and the origin of this gene in the evolutionary process. The other is the molecular and biochemical mechanisms underlying the interaction between the gene and the environment," said Prof. Fang.
In 2019, Prof. Fang's team published a research article in PNAS, pointing out that 18 genes in the genome of M. robertsii could be acquired via horizontal gene transfer transferred horizontally. Some of these "alien genes" from bacteria or arthropods can produce those substances that help break through the insect's body wall, thus equipping M. robertsii with an "ace in the hole"-the ability to penetrate the insect's "iron wall".
In the current study, Prof. Fang showcased two new "treasures" he found in M. robertsii: methylmercury demethylase (MMD) and mercury ion reductase (MIR). Mercury has different species with varying degrees of toxicity. Among them methylmercury is the most toxic, and when entering the body, it will spread throughout the body and cause irrevocable damage to the nervous system.
According to Prof. Fang, MMD is a demethylase, and it can degrade highly-toxic methylmercury into Hg2+, whereas the ion reductase MIR can reduce divalent mercury to volatile elemental mercury. The researchers found that among the 1.5 million-plus species of fungi on Earth, those species that possess both genes are exceedingly rare, and that merely Metarhizium fungi form reciprocal symbiotic relationship with plants. "This piques our curiosity. With these two genes, is M. robertsii really resistant to mercury?"
Schematic diagram of mechanism of how M. robertsii remediates mercury pollution in soil
The researchers simulated a mercury-contaminated zone in a petri dish, with 10 mg of methylmercury per liter of medium. Three strains of "martyr" M. robertsii were put to the test: the knocked-out strain, the wild-type strain and the enhanced strain. The results showed that the wild-type strain could grow basically normally in the hard-hit area, the knocked-out strain ended up dying of poisoning, and the enhanced strain displayed stronger vitality than the wild-type strain. The study confirmed that MMD and MIR could join hands to make mercury "invisible" and endowed M. robertsii with the capacity to contend with highly-toxic methylmercury.
M. robertsii can not only "detoxify the toxin for itself" but also "serve as a shield" for plants. The researchers also carried out experiments on wild-type-treated maize. The maize was vulnerable to methylmercury per se, but M. robertsii could remediate soil in a timely manner, thereby reducing the possibility that mercury entered plants. After 10 days, the mercury in the hard-hit area was gone and maize grew well.
Growth experiments of maize in mercury contaminated soil
Prof. Fang also paid much attention to severe mercury pollution. With the development of industry and agriculture and global warming, mercury pollution is posing an increasingly serious threat to human health and food security. For the present, this pollution is tackled primarily via physical and chemical solutions and plant adsorption, but these ways are either ineffective or costly.
Prof. Fang saw a spark of hope in M. robertsii. "Our experiments have demonstrated that M. robertsii can remediate mercury-polluted soil, reduce mercury accumulation in plants, and promote the health and growth of plants. When M. robertsii mycelia are put into mercury-polluted water, mercury pollution in fresh and salt water can also be remediated," said Prof. Fang. "The maintenance cost of M. robertsii is stunningly low. It can reproduce by feeding on the nutrients secreted by the plant root system." He believed that it would be an exceedingly feasible to involve M. robertsii in the treatment of contaminated soil in vast farmlands and forests.
Prof. FANG Weiguo (the first from the right) and his students in the lab
"Since M. robertsii is a biological control agent widely used in agriculture, its safety in the ecological environment has been confirmed and its mass production technology has grown to maturity. In the not-too-distant future, it can be applied to real-world scenarios," said Prof. Fang.
Image credit: ZHU Yuanzhi, WU Congcong
