Exserohilum rostratum, the killing fungus

There are hundreds of topics I could write about. The hardest part about writing is choosing a suitable topic and sticking with it until the end. This time, however, it was a little easier than normally due to the interesting nature of Exserohilum rostratum. Ever heard of it? It’s a fungus that seems to cause fatal meningitis, right now. Wait, right now?! Let’s find out what is going on.

It’s been a while since Charles Frank Drechsler (1923) described the ascomycete fungusHelminthosporium rostratum [1]. Then Stanley J. Hughes (1958) excluded from the genusHelminthosporium a group of graminicolous species corresponding to another genus, Ito’s Drechslera (1930). Robert A. Shoemaker (1959) described even a third genus Bipolaris to exclude species that were not like Drechslera from Helminthosporium. These genera have been rejected by different authors for various reasons and likewise, they have been accepted for various other reasons. Anyway, to make a long story short: the current accepted name for what we are talking about right now is Exserohilum rostratum.

It is interesting to consider that this fungus belongs to the Ascomycota. Members of this phylum go through asexual (anamorphic) phases during which they reproduce rapidly by mitospores or conidia (generated through the cellular process of mitosis). The sexual phase with the asci is called the teleomorph.

Back to Exserohilum rostratum, is this the anamorph or teleomorph? Let’s have a look at the original description of Helminthosporium rostratum [1].

Occurring on the dry leaves of Eragrostis major, host [current name: Eragrostis cilianensis, stinkgrass].

Conidiophores dark olivaceous, emerging singly or in groups of 2 to 5 from stomata or between epidermial cells, the swollen bases more or less united; measuring 6 to 8 by 40 to 180 µ; 1 to 6 septate, the septa separated by intervals of 15 to 40 µ; proliferating the first spore 40 to 140 µ from the base, and successive spores at intervals of 10 to 30 µ, at the apices of well-defined geniculations.

Conidia, when mature, dark olivaceous; straight or less frequently somewhat curved; often short, widest at or somewhat below the middle, tapering moderately or more markedly towards both ends, the hemispherical apex abruptly rounded off, the basal end somewhat more acute, often exhibiting a rounded conical contour; or less frequently produced at the tip into a more or less elongated rostrate prolongation.

There it is: Exserohilum rostratum (= Helminthosporium rostratum) is the asexual state, the anamorph, since its description is almost purely based on conidial characteristics.

An anamorph/teleomorph connection for this fungus was only made in 1976, when Setosphaeria rostrata K.J. Leonard was described and recognized as teleomorph of Exserohilum rostratum.

Biocontrol agent

Human impact on the natural environment has expanded tremendously over the past century. Rapid population growth and a globalized economy have caused widespread pollution, habitat destruction and climate change. One major but often little appreciated problem in our increasingly interconnected global biosphere is the ecological disturbance caused by animals and plants invading new ecosystems. Often these invasions occur unintentionally, for example through ships releasing their ballast water into foreign waters, or through worldwide trade in agricultural and horticultural products. Many other invasions result from deliberate introductions, which have run out of control.

Invading species disrupt the normal functioning of ecosystems by directly outcompeting native species, destabilizing food webs or affecting the cycling of nutrients through the ecosystem. Invasive species may drive native species to extinction through simple food competition, by using available food resources more efficiently, or by mating with native species to which they are closely related (hybridization). Invasive ‘alien’ species are now considered one of the top drivers for global biodiversity loss.

Red sprangletop, Leptochloa chinensi (Linnaeus) Nees, is a grassy weed originated in tropical Asia. It is distributed throughout Southeast Asia, from East Asia to South Africa, Burma, Sri Lanka, India, Australia, and Japan, where it is an ‘alien’ species. The weed has adapted to moist, swampy places in open habitats and is a huge seed producer (more than 40,000 seeds per plant). Therefore, it is a significant problem in rice, corn, sorghum, and soybean fields. This weed is a serious strain on rice yield. Annual worldwide rice yield loss caused by this weed is estimated to be between 15 – 21%. Now, our fungus of interest Exserohilum rostratum has recently been demonstrated to work as a biocontrol agent against red sprangletop through a two-phase system [2]:

In the first phase, quantitatively sufficient mycelia were cultured in submerged liquid culture. The basal medium contained 20 g of glucose, 2 g of NaNO₃, 1 g of K₂HPO₄, 1g of KH₂PO₄, 0.5g of MgSO₄, 0.2g of CaCl₂, 3.4g of polypeptone, 3.4g of yeast extract, 10g of rice oil, and 20g of polyurethane foam (5mm-cubes, Bridgestone Co. Ltd. Tokyo), which provide approximately 3,500 cubes per 1 L of distilled water. The initial pH was adjusted to 5.5 by 0.1 N HCl. Each 500mL-flask containing 150mL of the medium containing polyurethane foam was inoculated with 0.1% (v/v) conidia suspension obtained by plate culture. Following autoclaving, these flasks were incubated on a rotary shaker at 100rpm in the dark.

In the second phase, conidia were produced in the open air. After submerged in liquid culture, the sponge matrix covered with mycelia was separated from the culture broth through filtration using a sieve. To cause the conidiation of the fungus, mycelia on the surface of polyurethane foam were exposed to the air in a beaker at 25° C in a moist chamber.

The authors of this particular research even state that this “two-phase system […] may serve as a promising tool for mass-production of bioherbicides.”

However, there are two sides to every coin

On October 14, 2012 Federal officials reported contaminated injections had sickened 214 people in fifteen states. So far (October 25), 304 people have been diagnosed with meningitis, 23 of whom died, after having had steroid injections into the epidural space as a treatment for back pain. The injections were found to be contaminated with Exserohilum rostratum. This fungus thus seems to have some characteristics that we should take into account when considering using it as a biocontrol agent.

Exserohilum includes several saprobic species in the bark, leaves, and stems of both woody and herbaceous plants, but there’s also a large number of parasitic species. Those affecting graminaceous hosts are pretty well known, because of their possible use as effective biocontrol. Next to these economically important forms, many other species of Exserohilum are recorded as thriving on various members of the grass family, but have remained more or less obscure because either the hosts affected were of little economic value, or their parasitism caused little or no observable damage. I think ‘obscure’ is the correct word when thinking back to the 23 people who have died because of the injection of Exserohilum spores into the epidural space.

Although ubiquitous, members of the genus Exserohilum are rarely pathogenic for humans. Only three species have been shown to parasitize humans: E. rostratum, E. longirostratum and E. macginnisii [3]. The most common type of infections are sinusitis and skin infections, although also a few cases of cerebral abscesses, keratitis, osteomyelitis, prosthetic valve endocarditis and disseminated infection have been described.

In 2007 a child undergoing treatment for acute lymphoblastic leukemia (ALL) was infected by Exserohilum rostratum, causing cutaneous phaeohyphomycosis. The infection was due to contaminated intravenous dressings. In total, only ten cases of primary cutaneous skin infections due to Exserohilum have been described in the English literature. The problems with these reports are the incomplete data on follow-up and the lack of discussion of the potential use of newer antifungal agents. However, treatment of these cutaneous infections is primarily based on aggressive surgical removal combined with antifungal therapy.

The Centre Hospitalier Universitaire Saint-Justine (Montreal, Quebec) decided after the 2007 Exserohilum rostratum case to replace all wooden boards used to secure intravenous lines by Plexiglas covered with sterile gauze. The replacement occurred as part of an infection control policy and is said to be potentially lifesaving [3]. However, no fungal traces were found, although certain tapes and wooden devices have been reported to be linked with fungal infection.

Last month, 17 states reported cases with fungal meningitis. The outbreak was traced back toExserohilum rostratum contaminated medication for epidural steroid injections, packaged and marketed by the New England Compounding Center (Framingham, MA). It is estimated that more than 14,000 people may have been exposed to the contaminated medication – they are not necessarily infected.

As a conclusion we may want to limit working with Exserohilum rostratum. If this invasive Leptochloa weed is still bothering you, I suggest trying to raise a green manuring legume in the summer in crop fields that would be ploughed in situ at the time of preparing fields [4]. I’m sure this won’t kill you.

(DH, SciLogs.com)

References:

[1] Drechsler CF 1923, Journal of Agricultural Research 24: 641-740. [2] Yamaguchi K, Nagai K & E Matsumoto 2009. Bulletin of Minamikyushu University 39A: 73-77. [3] Saint-Jean M, St-Germain G, Lafarrière C & B Tapiero 2007. Canadian Journal of Infectious Diseases and Medical Microbiology 18: 200-202. [4] Kathiresan KR 2006. NIAES Symposium, Japan. [5] Leonard KJ 1976, Mycologia 68: 402-411.

I thank Sarah Verhaeghen, Rachel Engstrand and Donald H. Pfister for giving me valuable comments.

And last but not least, for the fans, I’ve got some pretty awesome taxonomy [5], just because I (and not only me, so it seems) like to explore the history of names:

Exserohilum rostratum (Drechsler) K.J. Leonard & Suggs, 1974, Mycologia 66: 290.

= Helminthosporium rostratum Drechsler, 1923, J. Agric. Res. 24: 724.

= Bipolaris rostrata (Drechsler) Shoemaker, 1959, Canad. J. Bot. 37: 883.

= Drechslera rostrata (Drechsler) Richardson & Fraser, 1968, Trans. Brit. Mycol. Soc. 51: 148.

= Exserohilum halodes (Drechsler) K.J. Leonard & Suggs, 1974, Mycologia 66: 290.

= Helminthosporium halodes Drechsler, 1923, J. Agric. Res. 24: 709.

= Bipolaris halodes (Drechsl.) Shoemaker, 1959, Canada. J. Bot. 37: 883.

= Drechslera halodes (Drechsl.) Subramanian & Jain, 1966, Current Sci. 35: 354.

= Helminthosporium halodes Drechsler var. tritici Mitra, 1931, Trans. Brit. Mycol. Soc. 15: 287.

= Helminthosporium halodes Drechsler var. elaeicola Kovachich, 1954, Trans. Brit. Mycol. Soc. 37: 423.