Who Dares Doubt The De­com­pos­ing Pow­ers Of Fungi?

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.

Fig­ure 1. Il­lus­tra­tion by Mary Par­rish, un­der the di­rec­tion of Tom Phillips and William DiMichele, pub­lished as fig­ure 22 in Willard DA, Phillips TL, Les­ni­kowska WA, and DiMichele WA. 2007. Pa­le­o­eco­logy of the Late Penn­syl­van­ian-Age Calh­o­un coal bed and im­pli­ca­tions for long-term dy­na­mics of wet­land eco­systems, In­tern. Jour­nal of Coal Ge­ol­ogy, 69:21 − 54. Source ETE pub­li­ca­tion 129

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.

Fig­ure 2. Mod­ern white rot, and Up­per De­von­i­an fos­sil wood spec­i­mens of Cal­lixy­lon new­ber­ry­i con­tain­ing fun­gal hy­phae or ex­hibit­ing pat­terns con­sis­tent with fun­gal de­cay. A Mod­ern wood ex­hibit­ing macro­scopic white rot de­cay pat­tern with patches of de­graded tis­sue. (Scale bar, 5 mm.) B Ac­etate peel of C. new­ber­ryi il­lus­trating ex­ten­sive macro­scopic de­cay con­sis­tent with fun­gal de­cay to the left of the ar­row. Spe­ci­men from Ket­tle Point, On­tario, United States Na­tional Mu­seum num­ber 618400. (Scale bar, 1 cm.) C Lon­gi­tu­di­nal thin sec­tion of C. new­ber­ryi wood and as­so­ci­ated fun­gal hy­phae pre­vi­ously de­scribed and rec­og­nized as con­sis­tent with white rot de­cay, al­though with­out do­cu­men­ta­tion of clamp con­nec­tions nec­es­sary for place­ment in Ba­sid­iomy­cota. (Scale bar, 25 µm.) Source

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.

 

Ref­er­ences

(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.