by David Lipson
Apparently, it is widely accepted that it took fungi 120 million years to figure out how to decompose woody plants. Hence lignin-rich materials accumulated along with the appearance of widespread forests in the Carboniferous Period (ca. 359 − 299 million years ago), which led to huge coal deposits until white rot fungi finally caught up in the Permian (ca. 299 − 252 mya). As a microbial chauvinist, I can't imagine fungi being this evolutionarily retarded. If alien plants composed of degradable plastic were to invade the Earth, would it take 120 million years to evolve efficient biodegradation pathways? My money is on centuries, maybe even decades. Look at xenobiotics like pentachlorophenol (PCP) that have only been around for a few decades: the current bacterial enzymes might be a little awkward, like an early generation cell phone, but they do the job.
Fortunately, this disconcerting situation has been rectified. Nelson et al. (1) debunk this evolutionary lag hypothesis with multiple lines of evidence. This study is essentially a thought experiment based on existing data and samples. Their primary finding was that coal accumulation was not dependent on lignin, but rather was driven mostly by non-lignified bark tissue from lycopsids, the dominant tree of the time. Therefore, lack of lignin decay could not be responsible for the Carboniferous coal deposits.
A simple mass balance approach shows that if all lignified plant tissues were to remain preserved for 120 million years, they would have become such a large carbon sink that atmospheric CO2 would have essentially vanished. There is abundant fossil evidence that vascular plant material deposited above the water table, and therefore exposed to oxygen, was subject to decay during this period. The authors review the molecular clock evidence for the appearance of the Agaricomycetes and other lignin-degrading organisms (which leads to an estimate centered in the Permian) and find there is much room for error, given uncertainties that could easily include the Carboniferous, not to mention fossils of decayed wood from well before the Permian (see Figure 2). They also point out the lignin-transforming enzymes other than fungal class II lignin peroxidases that are present in other fungal lineages and bacteria. As the authors say, "there appears to have been no shortage of options available for the decomposition of lignified tissue in the pre-Permian world." It was most likely the swampy, anoxic conditions of the time that led to preservation of plant matter in the form of peat, and the geological subsidence of the land that preserved the peat deposits and allowed them to form into coal. Not the fungi's fault.
Anyway, vascular plants didn't arrive in a space ship, preformed with xenobiotic lignin-reinforced xylem. They evolved from non-vascular plants with lignin-like molecules already in their cell walls (the complete lignin biosynthesis pathway is found in moss (2,3)), presumably plagued with pathogens and decomposed efficiently by the microbes of the period. Could plants have suddenly stumbled into an innovation that stumped fungi for 120 million years? Nope.
(1) Nelsen MP, DiMichele WA, Peters SE, Boyce CK. 2016. Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proc Natl Acad Sci USA, 113 (9), 2442 − 2447 PMID 26787881 (Open Access)
(2) Ligrone R, Carafa A, Duckett JG, Renzaglia KS, Ruel K. 2008. Immunocytochemical detection of lignin-related epitopes in cell walls in bryophytes and the charalean alga Nitella. Plant Systematics and Evolution, 270 (3,4), 257 − 272 JSTOR (Paywall)
(3) Xu Z, Zhang D, Hu J, Zhou X, Ye X, Reichel KL, Stewart NR, Syrenne RD, Yang X, Gao P, Shi W, Doeppke C, Sykes RW, Burris JN, Bozell JJ, Cheng MZ, Hayes DG, Labbe N, Davis M, Stewart CN Jr, Yuan JS. 2009. Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinformatics, 10, Suppl 11:S3 PMID 19811687 (Open Access)
David Lipson works on plant-microbe interactions and teaches microbiology as associate professor at USCD, San Diego. He also takes what he's learned as a microbiologist and applies it to the design of microtonal guitars that deviate from the standard 12-note system by removing the frets from various electric and acoustic guitars and repositioning them to create novel scales.