Fungus Fights Back

Fungi come in diverse colors: black, green, white, pink, yellow, red, and many more. Equally diverse are their shapes and sizes, from single-celled yeasts and fuzzy molds, to large mushrooms. They are found everywhere – at home, at the workplace, and of course outside – even if you cannot see them. What’s more, they even grow in harsh environments such as deserts and radioactive surroundings. Although thousands of species have been characterized, there are over a million species of fungi, most of which are waiting to be discovered. They are armed with remarkable abilities to guard themselves from enemies – one of the keys to their success.

Different types of fungi  Image Source: Wikipedia

Different types of fungi
Image: Wikipedia

Fungi are a good source of nutrients and fungivores, akin to herbivores, are organisms that primarily feed on fungi. Most fungivores are insects but there are also some small mammals, for example, the northern flying squirrel. From the viewpoint of fungi, fungivores present a threat to their survival, and they ought to protect themselves.

How do they defend themselves from attack? One tactic is to produce chemicals known as secondary metabolites, which include toxins to deter fungivores from eating them. Sometimes these toxins, while harmful to the organisms against which they are produced, can be a boon to others. In fact, the most widely used antibiotic that has saved countless lives, namely penicillin, is a secondary metabolite produced by Penicillium fungi when their growth is restrained in stressful environments. Another secondary metabolite harnessed by scientists led to a whole class of drugs called statins – used to lower blood cholesterol – that rake in billions of dollars annually for pharmaceutical companies.

As producing secondary metabolites uses valuable cellular resources that could have otherwise been used for growth, it would be advantageous for fungi to produce them only when required – a phenomenon known as inducible resistance. While this process is well documented in plants, it is unclear if fungi defend themselves regardless of the presence of fungivores. Scientists in Germany decided to investigate this using Aspergillus nidulans, a filamentous mold – composed of long string-like filaments – and Drosophila melanogaster larvae, the fungivore, commonly known as the fruit fly. Drosophila larvae naturally feed on microfungi such as Aspergillus growing on plant material. Aspergilli are ubiquitous molds, found in soil, food, in or on plants, and even in paint; they are involved in degrading plant material.

Various Penicillium and Aspergillus spp grown in the lab  Image Source: Wikipedia

Various Penicillium and Aspergillus spp grown in the lab
Image: Wikipedia

Previous studies noted that when the fruit fly larvae feed on early-stage mold colonies to extract as much nutrients from them as possible, mold growth is adversely affected. However, the mold quickly recovers from the attack. Obviously, something is going on here.

What makes the mold recover? And are there any effects on the larvae after feeding on the mold? Scientists compared the mortality rates of larvae that grazed on three types of A. nidulans colonies: larvae-grazed colonies, undisturbed colonies, and artificially wounded colonies (created by touching needles to mimic chew marks). They found that larvae that grazed on colonies that were previously fed on by other larvae showed drastically higher mortality rates compared with the larvae that grazed on the other two colonies. It took only nine days from the time of exposure for all the larvae to die. Clearly, the mold was resisting further larval foraging by killing them. But, how does the mold exert its killer effect?

(A)D. melanogaster larvae around A. nidulans mold  (B)D. melanogaster wipe out A. nidulans mold exposing the agar on the dish  (C)A. nidulans growth in the absence of larvae  Image Source: Ortiz, Trienens, & Rohlfs, 2013

(A) D. melanogaster larvae around A. nidulans mold
(B) D. melanogaster wipe out A. nidulans mold exposing the agar on the dish
(C) A. nidulans growth in the absence of larvae
Image Source: Ortiz, Trienens, & Rohlfs, 2013

It is widely known among scientists that the activities of our genes, which are found in the DNA of every cell of our body, are responsible for many changes we see in our body. Some genes are turned on or their activity is cranked up in response to certain environmental changes while others are turned off or their activity is reduced. So, the researchers thought that the fungus’ genes might shed some light on the observations above.

To see what was going on in A. nidulans at the genetic level, the researchers quantified the mRNA, the cell’s machinery that copies the gene code from DNA and is used to make proteins. They focused on 13 genes in particular that might be involved in conferring the resistance induced by the larvae. These genes are involved in altering secondary metabolite production, oxylipin (an oxygenated fatty acid associated with stress response in plants) production, and various genes that regulate the expression of other genes involved in responding to stress. They found that 12 out of the 13 genes were expressed at considerably higher levels after grazing and they singled out a possible gene – laeA – suspected of causing the resistance. LaeA is part of a combination of proteins called the velvet complex and regulates secondary metabolite production in Aspergillus species.

To confirm if LaeA was in fact responsible for the resistance, they fed larvae two types of A. nidulans: a wild-type with laeA present and a laeA-deficient version. They monitored the growth of the larvae and the fungus. The results were surprising – all the larvae that fed on the wild-type strain died before reaching adult stage whereas those that fed on the laeA-deficient strain reached adult stage; but their survival was lower compared to larvae feeding on other food sources such as dietary yeast (larvae thrive when feeding on yeast).

The laeA-deficient A. nidulans was unable to recover from larval foraging compared with the wild-type. As a result, with time, the larvae devoured the fungus, that in turn decreased their own food source, and it took them longer to reach adult stage. In contrast, dietary yeast, which shares a favorable association with the larvae (they both are mutualistic), was able to flourish when the larvae used them as their sole food source. These results suggest that LaeA appears to be essential in shielding the fungus from D. melanogaster larvae by impairing the fitness of the larvae. Interestingly, laeA is conserved in filamentous fungi, meaning it is present in all filamentous fungi; chances of survival without it might have been low.

It’s no wonder that fungi have been on our planet for millions of years, with their rapid and insidious maneuvers to shield themselves from attack. This is just the tip of the iceberg – fungi have probably evolved countless defense strategies given their enormous diversity.

References

Caballero Ortiz S, Trienens M, Rohlfs M (2013) Induced Fungal Resistance to Insect Grazing: Reciprocal Fitness Consequences and Fungal Gene Expression in the DrosophilaAspergillus Model System. PLoS ONE 8(8): e74951. doi:10.1371/journal.pone.0074951

 

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