A comparison of lignin-degrading enzyme activities in forest floor layers across a global climatic gradient

Abstract

Rapid litter turnover in tropical forests and during summer seasons might be due to increases in ligninolytic enzyme activities during warmer periods. We compared ligninolytic enzyme activity [lignin peroxidase (LiP), manganese peroxidase (MnP), and laccase (Lac)] in the organic layers of forest soils across a global climate gradient. As expected, MnP activities in fresh litter layers increased with increasing air temperature. Litter Mn/lignin ratios correlate positively with MnP activity and more rapid litter turnover in warmer climates. In contrast, LiP and Lac activities are regulated by site-specific conditions. Lac activity is commonly observed in less acidic fresh litter layers, while LiP activity localizes in acidified and lignin-rich deeper organic layers. The widespread occurrence of MnP and an increase in MnP activities in warmer climates support efficient lignin degradation in the tropics and during summer seasons. High Mn/lignin ratios in fresh litter could be an indicator of lignin degradability by MnP-producing fungi across global climate gradients.

Keywords

Acidification / Ligninolysis / Litter decomposition / Manganese / White-rot fungi

References

[1] Aerts, R., 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79, 439–449

[2] Allen, S.E., Grimshaw, H.M., Parkinson, J.A., Quarmby, C., 1974. Chemical Analysis of Ecological Materials. Wiley, New York.

[3] Anderson, J.P.E., Domsch, K.H., 1973. Quantification of bacterial and fungal contributions to soil respiration. Archives of Microbiology 93, 113–127.

[4] Archibald, F.S., 1992. A new assay for lignin-type peroxidases employing the dye azure B. Applied and Environmental Microbiology 58, 3110–3116

[5] Arora, D.S., Chander, M., Gill, P.K., 2002. Involvement of lignin peroxidase, manganese peroxidase and laccase in degradation and selective ligninolysis of wheat straw. International Biodeterioration & Biodegradation 50, 115–120

[6] Baldrian, P., 2006. Fungal laccases occurrence and properties. FEMS Microbiology Reviews 30, 215–242

[7] Berg, B., Steffen, K.T., McClaugherty, C., 2007. Litter decomposition rate is dependent on litter Mn concentrations. Biogeochemistry 82, 29–39

[8] Blair, J.M., 1988. Nitrogen, sulfur and phosphorus dynamics in decomposing deciduous leaf litter in the southern Appalachians. Soil Biology & Biochemistry 20, 693–701

[9] Bollag, J.M., Leonowicz, A., 1984. Comparative studies of extracellular fungal laccases. Applied and Environmental Microbiology 48, 849–854

[10] Bonnarme, P., Jeffries, T.W., 1990. Mn (II) regulation of lignin peroxidase and manganese-dependent peroxidase from lignin-degrading white rot fungi. Applied and Environmental Microbiology 56, 210–217

[11] Criquet, S., Farnet, A.M., Tagger, S., Le Petit, J., 2000. Annual variations of phenoloxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors. Soil Biology & Biochemistry 32, 1505–1513

[12] Criquet, S., Tagger, S., Vogt, G., Iacazio, G., Lepetit, J., 1999. Laccase activity of forest litter. Soil Biology & Biochemistry 31, 1239–1244

[13] Fioretto, A., Papa, S., Pellegrino, A., Fuggi, A., 2007. Decomposition dynamics of Myrtus communis and Quercus ilex leaf litter: Mass loss, microbial activity and quality change. Applied Soil Ecology 36, 32–40

[14] Fujii, K., Funakawa, S., Hayakawa, C., Kosaki, T., 2008. Contribution of different proton sources of pedogenetic soil acidification in forested ecosystems in Japan. Geoderma 144, 478–490

[15] Fujii, K., Hartono, A., Funakawa, S., Uemura, M., Kosaki, T., 2011. Acidification of tropical forest soils derived from serpentine and sedimentary rocks in East Kalimantan, Indonesia. Geoderma 160, 311–323

[16] Fujii, K., Hayakawa, C., 2020. Effects of land use change on turnover and storage of soil organic matter in a tropical forest. Plant and Soil 446, 425–439

[17] Fujii, K., Hayakawa, C., Inagaki, Y., Ono, K., 2019. Sorption reduces the biodegradation rates of multivalent organic acids in volcanic soils rich in short-range order minerals. Geoderma 333, 188–199

[18] Fujii, K., Morioka, K., Hangs, R., Funakawa, S., Kosaki, T., Anderson, D.W., 2013b. Importance of climate and parent material on soil formation in Saskatchewan, Canada as revealed by soil solution studies. Pedologist 57, 27–44.

[19] Fujii, K., Shibata, M., Kitajima, K., Ichie, T., Kitayama, K., Turner, B.L., 2018. Plant–soil interactions maintain biodiversity and functions of tropical forest ecosystems. Ecological Research 33, 149–160

[20] Fujii, K., Uemura, M., Hayakawa, C., Funakawa, S., Kosaki, T., 2013a. Environmental control of lignin peroxidase, manganese peroxidase, and laccase activities in forest floor layers in humid Asia. Soil Biology & Biochemistry 57, 109–115

[21] Glenn, J.K., Gold, M.H., 1985. Purification and properties of an extracellular Mn (II)-dependent peroxidase from the lignin-degrading basidiomycete, Phanerochaete chrysosporium. Archives of Biochemistry and Biophysics 242, 329–341

[22] Gower, S.T., Vogel, J.G., Norman, J.M., Kucharik, C.J., Steele, S.J., Stow, T.K., 1997. Carbon distribution and aboveground net primary production in aspen, jack pine, and black spruce stands in Saskatchewan and Manitoba, Canada. Journal of Geophysical Research, D, Atmospheres 102, 29029–29041

[23] Hatakka, A., (2001) Biodegradation of lignin. In: Hofrichter, M., Steinbüchel, A., eds. Biopolymers: Biology, Chemistry, Biotechnology, Applications, vol 1. Lignin, Humic Substances and Coal. Wiley VCH, Weinheim, pp. 129–180.

[24] Hofrichter, M., 2002. Review: lignin conversion by manganese peroxidase (MnP). Enzyme and Microbial Technology 30, 454–466

[25] Inagaki, Y., Inagaki, M., Hashimoto, T., Kobayashi, M., Ito, Y., Shinomiya, Y., Yoshinaga, S., 2012. Aboveground production and nitrogen utilization in nitrogen-saturated coniferous plantation forests on the periphery of the Kanto Plain. Bull FFPRI 424, 161–173.

[26] Joergensen, R.G., Wichern, F., 2008. Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology & Biochemistry 40, 2977–2991

[27] Kamei, I., Daikoku, C., Tsutsumi, Y., Kondo, R., 2008. Saline-dependent regulation of manganese peroxidase genes in the hypersaline-tolerant white rot fungus Phlebia sp. strain MG-60. Applied and Environmental Microbiology 74, 2709–2716

[28] Kellner, H., Luis, P., Pecyna, M.J., Barbi, F., Kapturska, D., Krüger, D., Zak, D.R., Marmeisse, R., Vandenbol, M., Hofrichter, M., 2014. Widespread occurrence of expressed fungal secretory peroxidases in forest soils. PLoS One 9, e95557

[29] Kirk, T.K., 1984, Degradation of lignin. In: Gibson, D.T., ed. Microbial Degradation of Organic Compounds. Marcel Dekker, New York, pp, 399–437.

[30] Kirk, T.K., Farrell, R.L., 1987. Enzymatic “combustion”: the microbial degradation of lignin. Annual Review of Microbiology 41, 465–505

[31] Leonowics, A., Cho, N.S., Luterek, J., Wilkolazka, A., Wojtas-Wasilewska, M., Matuszewska, A., Hofrichter, M., Wesenberg, D., Rogalski, J., 2001. Fungal laccase: properties and activity on lignin. Journal of Basic Microbiology 41, 185–227

[32] Maisto, G., Baldantoni, D., De Marco, A., Alfani, A., Virzo De Santo, A., 2013. Ranges of nutrient concentrations in Quercus ilex leaves at natural and urban sites. Journal of Plant Nutrition and Soil Science 176, 801–808.

[33] Meentemeyer, V., 1978. Macroclimate and lignin control of litter decomposition rates. Ecology 59, 465–472

[34] Megonigal, J.P., Conner, W.H., Kroeger, S., Sharitz, R.R., 1997. Aboveground production in southeastern floodplain forests: a test of the subsidy–stress hypothesis. Ecology 78, 370–384.

[35] Mikan, C.J., Schimel, J.P., Doyle, A.P., 2002. Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biology & Biochemistry 34, 1785–1795

[36] Moore, T.R., Trofymow, J.A., Prescott, C.E., Fyles, J., Titus, B.D., 2006. Patterns of carbon, nitrogen and phosphorus dynamics in decomposing foliar litter in Canadian forests. Ecosystems (New York, N.Y.) 9, 46–62

[37] Morgenstern, I., Klopman, S., Hibbett, D.S., 2008. Molecular evolution and diversity of lignin degrading heme peroxidases in the Agaricomycetes. Journal of Molecular Evolution 66, 243–257

[38] Nakane, K., Kohno, T., Horikoshi, T., Nakatsubo, T., 1997. Soil carbon cycling at a black spruce (Picea mariana) forest stand in Saskatchewan, Canada. Journal of Geophysical Research, D, Atmospheres 102, 28785–28793

[39] Olson, J.S., 1963. Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44, 322–331

[40] Orth, A.B., Royse, D.J., Tien, M., 1993. Ubiquity of lignin-degrading peroxidases among various wood-degrading fungi. Applied and Environmental Microbiology 59, 4017–4023

[41] Osono, T., 2007. Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecological Research 22, 955–974

[42] Oyadomari, M., Shinohara, H., Johjima, T., Wariishi, H., Tanaka, H., 2003. Electrochemical characterization of lignin peroxidase from the white-rot basidiomycete Phanerochaete chrysosporium. Journal of Molecular Catalysis. B, Enzymatic 21, 291–297

[43] Rothschild, N., Levkowitz, A., Hadar, Y., Dosoretz, C.G., 1999. Manganese deficiency can replace high oxygen levels needed for lignin peroxidase formation by Phanerochaete chrysosporium. Applied and Environmental Microbiology 65, 483–488

[44] Rüttimann-Johnson, C., Cullen, D., Lamar, R.T., 1994. Manganese peroxidases of the white rot fungus Phanerochaete sordida. Applied and Environmental Microbiology 60, 599–605

[45] Shibata, M., Sugihara, S., Mvondo-Ze, A.D., Araki, S., Funakawa, S., 2017. Nitrogen flux patterns through Oxisols and Ultisols in tropical forests of Cameroon, Central Africa. Soil Science and Plant Nutrition 63, 306–317

[46] Sinsabaugh, R.L., 2010. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology & Biochemistry 42, 391–404

[47] Slessarev, E.W., Lin, Y., Bingham, N.L., Johnson, J.E., Dai, Y., Schimel, J.P., Chadwick, O.A., 2016. Water balance creates a threshold in soil pH at the global scale. Nature 540, 567–569

[48] Šnajdr, J., Valášková, V., Merhautová, V., Herinková, J., Cajthaml, T., Baldrian, P., 2008. Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biology & Biochemistry 40, 2068–2075

[49] Staaf, H., 1987. Foliage litter turnover and earthworm populations in three beech forests of contrasting soil and vegetation types. Oecologia 72, 58–64

[50] Ten Have, R., Teunissen, P.J.M., 2001. Oxidative mechanisms involved in lignin degradation by white rot fungi. Chemical Reviews 101, 3397–3413

[51] Tien, M., Kirk, T.K., 1983. Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science 221, 661–662

[52] Trumbore, S., 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 10, 399–411

[53] Tuomela, M., Oivanen, P., Hatakka, A., 2002. Degradation of synthetic ¹⁴C-lignin by white-rot fungi in soil. Soil Biology & Biochemistry 34, 1613–1620

[54] Wong, D.W.S., 2009. Structure and action mechanism of ligninolytic enzymes. Applied Biochemistry and Biotechnology 157, 174–209

[55] Yasuda, Y., Saito, T., Hoshino, D., Ono, K., Ohtani, Y., Mizoguchi, Y., Morisawa, T., 2012. Carbon balance in a cool–temperate deciduous forest in northern Japan: seasonal and interannual variations, and environmental controls of its annual balance. Journal of Forest Research 17, 253–267

[56] Yoshida, M., Hashimoto, K., Iahimori, A., Nakada, Y., Hashimoto, K., Osaka, N., 2011. Detection of the genes encoding lignin and manganese peroxidases from white rot fungi. Wood Preservation 37, 111–121

Acknowledgments

We thank the Kinki and Chugoku Regional Forest Office of the Ministry of Agriculture, Forestry and Fisheries of Japan and the Experimental Forest of the Tropical Rainforest Research Center at Mulawarman University for allowing us to conduct studies at the experimental sites.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-020-0042-6 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2020 Higher Education Press