Microbial perspective of inhibited carbon turnover in Tangel humus of the Northern Limestone Alps.


Journal

Environmental microbiology reports
ISSN: 1758-2229
Titre abrégé: Environ Microbiol Rep
Pays: United States
ID NLM: 101499207

Informations de publication

Date de publication:
07 Dec 2023
Historique:
received: 14 06 2023
accepted: 01 11 2023
medline: 8 12 2023
pubmed: 8 12 2023
entrez: 8 12 2023
Statut: aheadofprint

Résumé

Tangel humus primarily occurs in montane and subalpine zones of the calcareous Alps that exhibit low temperatures and high precipitation sums. This humus form is characterized by inhibited carbon turnover and accumulated organic matter, leading to the typical thick organic layers. However, the reason for this accumulation of organic matter is still unclear, and knowledge about the microbial community within Tangel humus is lacking. Therefore, we investigated the prokaryotic and fungal communities along with the physical and chemical properties within a depth gradient (0-10, 10-20, 20-30, 30-40, 40-50 cm) of a Tangel humus located in the Northern Limestone Alps. We hypothesized that humus properties and microbial activity, biomass, and diversity differ along the depth gradient and that microbial key players refer to certain humus depths. Our results give the first comprehensive information about microbiota within the Tangel humus and establish a microbial zonation of the humus. Microbial activity, biomass, as well as microbial alpha diversity significantly decreased with increasing depths. We identified microbial biomarkers for both, the top and the deepest depth, indicating different, microbial habitats. The microbial characterization together with the established nutrient deficiencies in the deeper depths might explain reduced C-turnover and Tangel humus formation.

Identifiants

pubmed: 38062558
doi: 10.1111/1758-2229.13215
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Universität Innsbruck

Informations de copyright

© 2023 The Authors. Environmental Microbiology Reports published by Applied Microbiology International and John Wiley & Sons Ltd.

Références

Abarenkov, K., Zirk, A., Piirmann, T., Pöhönen, R., Ivanov, F., Nilsson, R. H., & Kõljalg, U. (2020). UNITE mothur release for Fungi [Data set]. UNITE Community. https://doi.org/10.15156/BIO/786381
Abera, G., Wolde-meskel, E. & Bakken, L.R. (2012) Carbon and nitrogen mineralization dynamics in different soils of the tropics amended with legume residues and contrasting soil moisture contents. Biology and Fertility of Soils, 48(1), 51-66.
An, J., Liu, C., Wang, Q., Yao, M., Rui, J., Zhang, S., & Li, X. (2019). Soil bacterial community structure in Chinese wetlands. Geoderma, 337, 290-299. https://doi.org/10.1016/j.geoderma.2018.09.035
Anderson, J.P.E. & Domsch, K.H. (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biology and Biochemistry, 10(3), 215-221.
Andreetta, A., Macci, C., Ceccherini, M.T., Cecchini, G., Masciandaro, G., Pietramellara, G. et al. (2012) Microbial dynamics in Mediterranean Moder humus. Biology and Fertility of Soils, 48(3), 259-270.
Bai, Z., Liang, C., Bodé, S., Huygens, D. & Boeckx, P. (2016) Phospholipid 13C stable isotopic probing during decomposition of wheat residues. Applied Soil Ecology, 98, 65-74.
Bell, T., Newman, J.A., Silverman, B.W., Turner, S.L. & Lilley, A.K. (2005) The contribution of species richness and composition to bacterial services. Nature, 436(7054), 1157-1160.
Berger, T.W., Duboc, O., Djukic, I., Tatzber, M., Gerzabek, M.H. & Zehetner, F. (2015) Decomposition of beech (Fagus sylvatica) and pine (Pinus nigra) litter along an alpine elevation gradient: decay and nutrient release. Geoderma, 251-252, 92-104.
Blum, W.E.H. (2020) Bodenkunde in Stichworten, 7. neu bearbeitete und ergänzte, Auflage edition. Stuttgart: Schweizerbart Textbooks, p. 195.
Bottino, F., Cunha-Santino, M.B. & Bianchini, I. (2016) Cellulase activity and dissolved organic carbon release from lignocellulose macrophyte-derived in four trophic conditions. Brazilian Journal of Microbiology, 47(2), 352-358.
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J. et al. (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences, 108(Supplement 1), 4516-4522.
Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K. et al. (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84(1), 45-67.
Cheng, F., Peng, X., Zhao, P., Yuan, J., Zhong, C., Cheng, Y. et al. (2013) Soil microbial biomass, basal respiration and enzyme activity of main forest types in the Qinling Mountains. PLoS One, 8(6), e67353.
Cleveland, C.C. & Liptzin, D. (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry, 85(3), 235-252.
Cleveland, C.C., Nemergut, D.R., Schmidt, S.K. & Townsend, A.R. (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry, 82(3), 229-240.
Clocchiatti, A., Hannula, E.S., Hundscheid, M.P.J., Gunnewiek, K., Paulien, J.A. & de Boer, W. (2021) Stimulated saprotrophic fungi in arable soil extend their activity to the rhizosphere and root microbiomes of crop seedlings. Environmental Microbiology, 23(10), 6056-6073.
Crow, S.E., Lajthal, K., Filley, T.R., Swanston, C.W., Bowden, R.D. & Caldwell, B.A. (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Global Change Biology, 15(8), 2003-2019.
DeBruyn, J.M., Nixon, L.T., Fawaz, M.N., Johnson, A.M. & Radosevich, M. (2011) Global biogeography and quantitative seasonal dynamics of gemmatimonadetes in soil. Applied and Environmental Microbiology, 77(17), 6295-6300.
Domeignoz-Horta, L.A., Shinfuku, M., Junier, P., Poirier, S., Verrecchia, E., Sebag, D. et al. (2021) Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence. ISME Communications, 1(1), 1-4.
Eilers, K.G., Debenport, S., Anderson, S. & Fierer, N. (2012) Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biology and Biochemistry, 50, 58-65.
Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M.M. et al. (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature, 464(7288), 543-548.
Fierer, N., Bradford, M.A. & Jackson, R.B. (2007) Toward an ecological classification of soil bacteria. Ecology, 88(6), 1354-1364.
Forest Site Classification Tyrol (2018) Waldtypisierung Tirol. Office of the Tyrolean Government, Innsbruck, AT.
Ghyselinck, J., Pfeiffer, S., Heylen, K., Sessitsch, A. & Vos, P.D. (2013) The effect of primer choice and short read sequences on the outcome of 16S rRNA gene based diversity studies. PLoS One, 8(8), e71360.
Giesler, R., Andersson, T., Lövgren, L. & Persson, P. (2005) Phosphate sorption in aluminum- and iron-rich humus soils. Soil Science Society of America Journal, 69(1), 77-86. Available from: https://doi.org/10.2136/sssaj2005.0077a
Gorfer, M., Borruso, L., Deltedesco, E., Gichuhi, E.W., Menge, D.M., Makihara, D. et al. (2022) The effect of environmental parameters and fertilization practices on yield and soil microbial diversity in a Kenyan paddy rice field. Applied Soil Ecology, 176, 104495.
Graham, E.D. & Tully, B.J. (2021) Marine dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. The ISME Journal, 15(4), 1248-1256.
Grand, S. & Lavkulich, L.M. (2011) Depth distribution and predictors of soil organic carbon in podzols of a forested watershed in southwestern Canada. Soil Science, 176(4), 164-174.
Hofmann, K., Praeg, N., Mutschlechner, M., Wagner, A.O. & Illmer, P. (2016) Abundance and potential metabolic activity of methanogens in well-aerated forest and grassland soils of an alpine region. FEMS Microbiology Ecology, 92(2), fiv171.
Hsieh, T.C., Ma, K.H. & Chao, A. (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12), 1451-1456.
Huse, S.M., Welch, D.M., Morrison, H.G. & Sogin, M.L. (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environmental Microbiology, 12(7), 1889-1898.
Illmer, P. & Schinner, F. (1995) Solubilization of inorganic calcium phosphates-solubilization mechanisms. Soil Biology and Biochemistry, 27(3), 257-263.
IUSS Working Group WRB. (2014) World reference base for soil resources 2014: international soil classification system for naming soils and creating legends for soil maps. World soil resources reports 106. Rome: FAO, p. 203.
Jastrow, J.D., Amonette, J.E. & Bailey, V.L. (2007) Mechanisms controlling soil carbon turnover and their potential application for enhancing carbon sequestration. Climatic Change, 80(1), 5-23.
Kirkby, C.A., Richardson, A.E., Wade, L.J., Passioura, J.B., Batten, G.D., Blanchard, C. et al. (2014) Nutrient availability limits carbon sequestration in arable soils. Soil Biology and Biochemistry, 68, 402-409.
Köberl, M., Wagner, P., Müller, H., Matzer, R., Unterfrauner, H., Cernava, T. et al. (2020) Unraveling the complexity of soil microbiomes in a large-scale study subjected to different agricultural management in Styria. Frontiers in Microbiology, 11,1052.
Kögel-Knabner, I. (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biology and Biochemistry, 34(2), 139-162.
Kolb, E. & Baier, R. (Eds.). (2001) Tangel-die wenig bekannte Humusform. Exkursionsführer zur Jahrestagung der Arbeitsgemeinschaft Forstliche Standorts- Und Vegetationskunde (AFSV) im Werdenfelser Land 19. 22.09.2001.
Kolb, E. & Kohlpaintner, M. (2018) Tangel humus forms-genesis and co-evolution with vegetation. Applied Soil Ecology, 123, 622-626.
Kraft, B., Jehmlich, N., Larsen, M., Bristow, L.A., Könneke, M., Thamdrup, B. et al. (2022) Oxygen and nitrogen production by an ammonia-oxidizing archaeon. Science, 375(6576), 97-100.
Leifeld, J., Bassin, S., Conen, F., Hajdas, I., Egli, M. & Fuhrer, J. (2013) Control of soil pH on turnover of belowground organic matter in subalpine grassland. Biogeochemistry, 112(1-3), 59-69.
Lemos, L.N., Medeiros, J.D., Dini-Andreote, F., Fernandes, G.R., Varani, A.M., Oliveira, G. et al. (2019) Genomic signatures and co-occurrence patterns of the ultra-small Saccharimonadia (phylum CPR/Patescibacteria) suggest a symbiotic lifestyle. Molecular Ecology, 28(18), 4259-4271.
Liebmann, P., Wordell-Dietrich, P., Kalbitz, K., Mikutta, R., Kalks, F., Don, A. et al. (2020) Relevance of aboveground litter for soil organic matter formation-a soil profile perspective. Biogeosciences, 17(12), 3099-3113.
Liu, C., Cui, Y., Li, X. & Yao, M. (2021) microeco: an R package for data mining in microbial community ecology. FEMS Microbiology Ecology, 97(2), fiaa255.
Liu, C.M., Kachur, S., Dwan, M.G., Abraham, A.G., Aziz, M., Hsueh, P.-R. et al. (2012) FungiQuant: a broad-coverage fungal quantitative real-time PCR assay. BMC Microbiology, 12(1), 1-11.
Lücker, S., Wagner, M., Maixner, F., Pelletier, E., Koch, H., Vacherie, B. et al. (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. PNAS, 107(30), 13479-13484.
Malik, A.A., Chowdhury, S., Schlager, V., Oliver, A., Puissant, J., Vazquez, P.G.M. et al. (2016) Soil fungal:bacterial ratios are linked to altered carbon cycling. Frontiers in Microbiology, 7, 1247.
Maron, P.-A., Sarr, A., Kaisermann, A., Lévêque, J., Mathieu, O., Guigue, J. et al. (2018) High microbial diversity promotes soil ecosystem functioning. Applied and Environmental Microbiology, 84(9), e02738-17.
Martinez, C.M., Alvarez, L.H., Celis, L.B. & Cervantes, F.J. (2013) Humus-reducing microorganisms and their valuable contribution in environmental processes. Applied Microbiology and Biotechnology, 97(24), 10293-10308.
Mašínová, T., Yurkov, A. & Baldrian, P. (2018) Forest soil yeasts: decomposition potential and the utilization of carbon sources. Fungal Ecology, 34, 10-19.
McMurdie, P.J. & Holmes, S. (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217.
McNamara, J.T., Morgan, J.L.W. & Zimmer, J. (2015) A molecular description of cellulose biosynthesis. Annual Review of Biochemistry, 84, 895-921.
Millanes, A.M., Diederich, P., Ekman, S. & Wedin, M. (2011) Phylogeny and character evolution in the jelly fungi (Tremellomycetes, Basidiomycota, Fungi). Molecular Phylogenetics and Evolution, 61(1), 12-28.
Murphy, C.L., Yang, R., Decker, T., Cavalliere, C., Andreev, V., Bircher, N. et al. (2021) Genomes of novel myxococcota reveal severely curtailed machineries for predation and cellular differentiation. Applied and Environmental Microbiology, 87(23), e0170621.
Neina, D. (2019) The role of soil pH in plant nutrition and soil remediation. Applied and Environmental Soil Science, 2019, 5794869.
Nunan, N., Schmidt, H. & Raynaud, X. (2020) The ecology of heterogeneity: soil bacterial communities and C dynamics. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 375(1798), 20190249.
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R. & Legendre, P.D.M. (2019) vegan: Community Ecology Package.
Olleck, M., Kohlpaintner, M., Mellert, K.H., Reger, B., Göttlein, A. & Ewald, J. (2021) Thick forest floors in the Calcareous Alps-distribution, ecological functions and carbon storage potential. Catena, 207, 105664.
Olleck, M., Reger, B. & Ewald, J. (2020) Plant indicators for Folic Histosols in mountain forests of the Calcareous Alps. Applied Vegetation Science, 23(2), 285-296.
Olleck, M., Reger, B. & Ewald, J. (2022) Humuspflege in Gebirgswäldern der Kalkalpen: Wissensstand und Massnahmen. Schweizerische Zeitschrift fur Forstwesen, 173(1), 36-43.
Orschler, L., Agrawal, S. & Lackner, S. (2019) On resolving ambiguities in microbial community analysis of partial nitritation anammox reactors. Scientific Reports, 9(1), 1-10.
Pascault, N., Ranjard, L., Kaisermann, A., Bachar, D., Christen, R., Terrat, S. et al. (2013) Stimulation of different functional groups of bacteria by various plant residues as a driver of soil priming effect. Ecosystems, 16(5), 810-822.
Ponge, J.-F., Zanella, A., Sartori, G. & Jabiol, B. (2010) Terrestrial humus forms: ecological relevance and classification. Villeurbanne: Centre pour la communication scientifique directe, hal.archives-ouvertes.fr. https://about.hal.science/en/
Praeg, N., Pauli, H. & Illmer, P. (2019) Microbial diversity in bulk and rhizosphere soil of Ranunculus glacialis along a high-alpine altitudinal gradient. Frontiers in Microbiology, 10, 1429.
Praeg, N., Schachner, I., Schuster, L. & Illmer, P. (2021) Carbon-dependent growth, community structure and methane oxidation performance of a soil-derived methanotrophic mixed culture. FEMS Microbiology Letters, 368(2), fnaa212 .
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P. et al. (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590-D596.
R Core Team. (2020) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: https://www.R-project.org/ [Accessed May, 2022]
Rasigraf, O., Kool, D.M., Jetten, M.S.M., Sinninghe Damsté, J.S. & Ettwig, K.F. (2014) Autotrophic carbon dioxide fixation via the Calvin-Benson-Bassham cycle by the denitrifying methanotroph “Candidatus Methylomirabilis oxyfera”. Applied and Environmental Microbiology, 80(8), 2451-2460.
Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584.
Rousk, J., Brookes, P.C. & Bååth, E. (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Applied and Environmental Microbiology, 75(6), 1589-1596.
Saghaï, A., Banjeree, S., Degrune, F., Edlinger, A., García-Palacios, P., Garland, G. et al. (2021) Diversity of archaea and niche preferences among putative ammonia-oxidizing Nitrososphaeria dominating across European arable soils. Environmental Microbiology, 24(1), 341-356.
Schinner, F. (Ed.). (1996) Methods in soil biology. Springer LAB manual. Berlin: Springer, p. 426.
Schleper, C., Jurgens, G. & Jonuscheit, M. (2005) Genomic studies of uncultivated archaea. Nature Reviews. Microbiology, 3(6), 479-488.
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B. et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537-7541.
Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S. et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biology, 12(6), R60.
Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X. et al. (2011) Phosphorus dynamics: from soil to plant. Plant Physiology, 156(3), 997-1005.
Soong, J.L., Fuchslueger, L., Marañon-Jimenez, S., Torn, M.S., Janssens, I.A., Penuelas, J. et al. (2020) Microbial carbon limitation: the need for integrating microorganisms into our understanding of ecosystem carbon cycling. Global Change Biology, 26(4), 1953-1961.
Turner, B.L. (2010) Variation in pH optima of hydrolytic enzyme activities in tropical rain forest soils. Applied and Environmental Microbiology, 76(19), 6485-6493.
Unterwurzacher, V., Pogner, C., Berger, H., Strauss, J., Strauss-Goller, S. & Gorfer, M. (2018) Validation of a quantitative PCR based detection system for indoor mold exposure assessment in bioaerosols. Environmental Science: Processes & Impacts, 20(10), 1454-1468.
van der Wal, A., Geydan, T.D., Kuyper, T.W. & de Boer, W. (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiology Reviews, 37(4), 477-494.
Vitorino, I.R. & Lage, O.M. (2022) The Planctomycetia: an overview of the currently largest class within the phylum planctomycetes. Antonie Van Leeuwenhoek, 115(2), 169-201.
Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E.E. & van der Heijden, M.G.A. (2019) Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nature Communications, 10, 4841.
Wang, L., Amelung, W., Prietzel, J. & Willbold, S. (2019) Transformation of organic phosphorus compounds during 1500 years of organic soil formation in Bavarian Alpine forests-a 31P NMR study. Geoderma, 340, 192-205.
Wang, N., Fu, Q., Zhou, Z., Shao, Y., Wang, J., Li, W. et al. (2021) Humus microhabitat affects distributions of soil fungi and bacteria in a temperate mountain forest. Ecology and Evolution, 11(13), 9148-9158.
Wang, Q., Garrity, G.M., Tiedje, J.M. & Cole, J.R. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267.
Westcott, S.L., Schloss, P.D., Watson, M. & Pollard, K. (2017) OptiClust, an improved method for assigning amplicon-based sequence data to operational taxonomic units. mSphere, 2(2), e00073-17.
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal rna genes for phylogenetics. In: PCR protocols, New York: Academic Press, Inc. pp. 315-322.
Wiegand, S., Jogler, M. & Jogler, C. (2018) On the maverick planctomycetes. FEMS Microbiology Reviews, 42(6), 739-760.
Xu, C.-Y., Du, C., Jian, J.-S., Hou, L., Wang, Z.-K., Wang, Q. et al. (2021) The interplay of labile organic carbon, enzyme activities and microbial communities of two forest soils across seasons. Scientific Reports, 11(1), 1-12.
Yu, Y., Lee, C., Kim, J. & Hwang, S. (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnology and Bioengineering, 89(6), 670-679.
Yun, J., Chen, X., Liu, S. & Zhang, W. (2019) Effects of temperature and moisture on soil organic carbon mineralization. IOP Conference Series: Materials Science and Engineering, 562(1), 12085.
ZAMG, ARPAV, Institut für Interdisziplinäre Gebirgsforschung IGF. (2015) Das Klima von Tirol-Südtirol-Belluno.
Zanella, A., Jabiol, B., Ponge, J.-F., Sartori, G., de Waal, R., van Delft, B., et al. (2011) European humus forms reference base. Villeurbanne:: Centre pour la communication scientifique directe, hal.archives-ouvertes.fr.
Zanella, A., Ponge, J.-F. & Briones, M.J.I. (2018) Humusica 1, article 8: terrestrial humus systems and forms-biological activity and soil aggregates, space-time dynamics. Applied Soil Ecology, 122, 103-137.
Zanella, A., Ponge, J.-F., Jabiol, B., Sartori, G. & Viola, F. (2018) Humusica 1, article 5: terrestrial humus systems and forms-keys of classification of humus systems and forms. Applied Soil Ecology, 122(Part 1), 75-86.

Auteurs

Theresa Rzehak (T)

Department of Microbiology, Universität Innsbruck, Innsbruck, Austria.

Nadine Praeg (N)

Department of Microbiology, Universität Innsbruck, Innsbruck, Austria.

Harald Zink (H)

Department of Geography, Universität Innsbruck, Innsbruck, Austria.

Alois Simon (A)

Department of Forest Planning, Office of the Tyrolean Government, Innsbruck, Austria.

Clemens Geitner (C)

Department of Geography, Universität Innsbruck, Innsbruck, Austria.

Paul Illmer (P)

Department of Microbiology, Universität Innsbruck, Innsbruck, Austria.

Classifications MeSH