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Divine intervention via a microbe

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The best science stories I hear about generally involve going back and reconciling or correcting observations from the past to unlock some new level of understanding. There are many such examples which exist only because time provides us with the tools to arrive at a correct answer where our ancestors could not. The best thing about these stories is that even though the exact answer might be wrong the clues provided by the old observations allow modern researchers to play detective to find new solutions to old questions.

One of my favourite stories concerns "angel glow". Reports of this particular phenomenon can be found from as far back as the U.S. Civil War and World War I, with reports of a mysterious blue glow in the open wounds of some injured soldiers. Why Angel Glow? Because these soldiers were less likely to suffer from infections often leading to sepsis and death, hence the "angel," and at night their wounds glowed an angelic luminescent blue, accounting for the ‘glow’. In a time before the easy identification of microbial life it was much easier to label the blue healing glow divine intervention but of course there was more to the story.

So what could be causing a blue glow? There are many organisms that glow a wide variety of colours from glow-worms to krill to the jack-o'-lantern mushroom but these organisms have never been observed to induce the healing properties of the recorded angel glow (in fact jack-o'-lanterns are poisonous) so there had to be something else, perhaps something microbial.

Bioluminescent bacteria are perhaps more common than you would expect with many Dinoflagellates, Vibrionaceae and Enterobacteriaceae members exhibiting some bioluminescence. Still, the vast majority of bioluminescent species are marine organisms which doesn’t fit the historical record as the glowing soldiers were engaged primarily in trench warfare on inland battle lines. This leaves only terrestrial bioluminescent organisms.

To date only a very small number of bioluminescent organisms are known to live in an entirely terrestrial environment. There are even fewer bioluminescent land loving micro-organisms but two closely related species of bacteria Photorhabdus spp. and Xenorhabdus spp. are known to glow.

These organisms are soil borne nematode symbionts and widely distributed around the world. In terms of our story they seem to tick a lot of boxes but why would they glow? And how are they promoting healing?

Both of these questions are answered by the normal lifecycle of the bacteria.

Both Photorhabdus and the related Xenorhabdus live in the gut of nematode worms as symbionts. The nematodes hunt down insect larvae in soil or on plant surfaces where they will burrow into the larvae and invade the larvae’s blood (more accurately called the hemolymph in insects). Once in the blood the nematode regurgitates the bacteria, which quickly spread throughout the larvae releasing a cocktail of chemicals that quickly overcome the insect larvae.

The chemical cocktail is very important to the story as this cocktail contains toxins like the PirAB toxin, which is larvicidal, and broad spectrum anti-microbials such as the ST molecule and S- and R- type pyocins. In the lifecycle of the bacteria these compounds help to kill the insect larvae and then remove any microbial competition from the carcass. This then allows the nematode and bacteria to feast on what has now become an insect larva shaped sack full of nematodes and bacteria.

This continues until the larva is hollowed out and the nematodes and bacteria have consumed all of their prey. It’s at this point the nematodes start eating the bacteria. By consuming the bacteria and allowing them to re-colonise their gut the nematodes engage in a trade off, they have to carry the bacteria from prey to prey but in return the bacteria kill the insect and kill all other microbes that could potentially harm both the nematode and themselves.

The wounds of the soldiers healed faster and without infection because of this anti-microbial cocktail. The best thing about this unusual interaction is that both Photorhabdus and Xenorhabdus spp. are not very infectious to humans. So they keep the wound clean, then are promptly cleared by the immune system. Having said that, infections with these bacteria do occur and generally result in localised ulceration and require prior skin breakage to gain entry.

But we still haven’t covered why they glow. Research seems to indicate that this is a baiting mechanism used to tempt new prey. Individual bacteria do glow but are not terribly luminescent, but, during the hollowing out of the insect larvae the bacteria reach sufficient concentrations to produce a visible glow that is thought to attract nearby larvae making the next meal attracted to the carcass of the last.

It’s easy to see why, in the absence of a better explanation, an ethereal glowing wound that heals faster and cleaner than other soldier’s wounds could only be seen as divine intervention but in my humble opinion a bacteria that co-opts a nematode, kills, cleans and feasts on an insect and then attracts new prey by glowing is a more amazing story. Unfortunately we can never really know for sure, but in the absence of a better explanation I’m going to stick with this one.

References:

Forst, S., Dowds, B., Boemare, N. & Stackebrandt, E. (1997). Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51, 47-72.

Goodrich-Blair, H. & Clarke, D. J. (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64, 260-268.

Waterfield, N. R., Ciche, T. & Clarke, D. (2009). Photorhabdus and a host of hosts. Annu Rev Microbiol 63, 557-574.

Figure legends:

Figure 1: Glow worm: A female Common Glow-worm (Lampyris noctiluca) in the grass in Loudwater, Buckinghamshire. Author - Timo Newton-Syms via Wikimedia.org. Krill: (Many krill. Source: english Wikipedia, original upload 15 June 2005 by Lupo, Photographer: Jamie Hall. Image source: [PD-USGov-NOAA] Category:Euphausiacea, via Wikimedia.org. Jack-o'-lantern mushroom: Photographer - Kent Loeffler.

Figure 2: Insect larvae carcass containing nematodes and the bioluminescent Photorhadus luminescens. Photo courtesy of Prof Richard French-Constant of the University of Exeter, U.K.

About the Author: James Byrne is in his third year as a PhD candidate in the Discipline of Microbiology and Immunology at the University of Adelaide. His research interest concerns the function of the Polysaccharide Co-Polymerase proteins of S. pneumoniae and their interactions to control the biosynthesis of the capsular polysaccharide that encapsulate this bacterium. Using a combination of mutation screens, protein interaction analysis and in vitro assays James hope to better understand the role of these proteins and in particular the role of CpsC. A better understanding of these systems may allow for the development of novel antimicrobial agents aimed at disrupting the process of exopolysaccharide polymerisation and ligation, a known virulence factor in many organisms. James also writes and maintains the loosely infectious disease themed blog Disease of the Week!

The views expressed are those of the author and are not necessarily those of Scientific American.

The views expressed are those of the author and are not necessarily those of Scientific American.

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