Lignin: The Enigma Remains
We are used to thinking of design as a positive presence. What if the things we don't see are missing for a reason also? Lignin, a complex organic polymer found in wood, is the second most abundant biopolymer on the planet, and higher gram for gram in stored energy than the most abundant biopolymer, cellulose. Yet nothing living can use lignin as an energy source. Why?
Perhaps the answer is because the indigestibility of lignin may be an essential requirement for the balance of life. Lignin slows the degradation of wood, thus allowing the buildup of humus in the soil, which in turn permits plant growth and all resulting life that depends on plants. The reasons for its indigestibility, and their implications are discussed in a recently published paper by Leisola et al. at the open access journal BIO-Complexity.
This conclusion seems to have struck a nerve. Some people who have read the paper, or at least the introductory blog post, have felt compelled to respond by digging up examples of lignin degradation from the literature.
There are a few things to note in response. First, Dr. Matti Leisola, the primary author of the paper, has worked on this subject for decades, and is widely respected by his peers. He did not "overlook" any references concerning lignin degradation. This should have been clear to anyone reading the paper, as the following quote shows:
The degradation of lignin by white-rot fungi has some special and even strange features. Firstly, lignin is not degraded during fungal growth but only after nutrient depletion triggers secondary metabolism. This is strange since secondary metabolism is usually connected to biosynthetic reactions rather than degradative processes. Secondly, despite the fact that complete oxidation of lignin is highly exothermic, fungal degradation of lignin actually needs an energy source. It has been postulated that lignin degradation is too slow to serve as a source of metabolic energy. Hatakka and Hammel ponder the possibility that "if lignin fragments were metabolized intracellularly, at least some energy and carbon should be gained from lignin for the fungus, and the fungus should be able to grow on lignin". This is questionable since it is apparent that the faster lignin is degraded the more energy is needed. Under optimal aerobic culture conditions, one gram of fungal mycelia degrades one gram lignin in about 48 hours consuming one gram of glucose in the process (as an energy source). Once glucose is depleted, lignin degradation ceases completely. And finally, fungi use the same kinds of enzymes (peroxidases and laccases) to initiate lignin degradation that plants use to make lignin. We call these curious features the lignin enigma.In short, fungi can break down lignin but need glucose as an energy source to do so.
Online critics cite several papers to argue that lignin can be used as a sole carbon source. The first is a paper from 1950, "Growth of Polyporus versicolor in a medium with lignin as the sole carbon source" by Pelczar, Gottlieb and Day in Archives of Biochemistry, 25; 449-45. The critics apparently failed to note that, in this paper, glucose had to be added as an energy source in order for lignin to be digested. A later paper by the same authors reported failure to digest lignin without added glucose.
Dr. Leisola has worked with the laccase-producing white-rot fungus Polyporus versicolor, also known as Trametes versicolor. He states, "It [the fungus] does not eat lignin." For example, a 1993 paper in Applied Environmental Microbiology clearly says that nearly all of the carbon dioxide evolved by hard wood kraft pulp (lignin-containing) cultures came from the added glucose, indicating that the pulp is not an important source of carbon or energy. A more recent paper from 2007 also states that it has been "clearly shown that laccase [the enzyme responsible for lignin degradation] production is not associated with cell growth, indicating that this ligninolytic enzyme must be produced in the defined medium by a secondary metabolism."
Finally, the critics cite a 2012 paper that purports to describe the use of "lignin as a carbon source for the cultivation of some Rhodotorula species." Once again in this paper lignin was not the sole carbon source. Glucose was added to the medium and some important controls and measurements were not done. At best, the most they could show was modification of lignin, not complete digestion. The authors actually state that "grass lignin exhibited a slightly inhibitory character on the two strains of yeast."
Recognizing the significant untapped resource that lignin represents, people have tried for decades to find ways to produce something useful from it, without success. An organism that could grow on lignin or produce useful chemicals from it, or an enzyme system that digests it completely would be revolutionary and a discovery worth the Nobel Prize. There are specific reasons why this has never happened, however. Given lignin's significance for the biosphere, that may be a good thing indeed.