All Title Author
Keywords Abstract

PLOS ONE  2014 

Network Analysis Reveals Ecological Links between N-Fixing Bacteria and Wood-Decaying Fungi

DOI: 10.1371/journal.pone.0088141

Full-Text   Cite this paper   Add to My Lib

Abstract:

Nitrogen availability in dead wood is highly restricted and associations with N-fixing bacteria are thought to enable wood-decaying fungi to meet their nitrogen requirements for vegetative and generative growth. We assessed the diversity of nifH (dinitrogenase reductase) genes in dead wood of the common temperate tree species Fagus sylvatica and Picea abies from differently managed forest plots in Germany using molecular tools. By incorporating these genes into a large compilation of published nifH sequences and subsequent phylogenetic analyses of deduced proteins we verified the presence of diverse pools corresponding to functional nifH, almost all of which are new to science. The distribution of nifH genes strongly correlated with tree species and decay class, but not with forest management, while higher fungal fructification was correlated with decreasing nitrogen content of the dead wood and positively correlated with nifH diversity, especially during the intermediate stage of wood decay. Network analyses based on non-random species co-occurrence patterns revealed interactions among fungi and N-fixing bacteria in the dead wood and strongly indicate the occurrence of at least commensal relationships between these taxa.

References

[1]  Cornwell WK, Cornelissen JHC, Allison SD, Bauhus J, Eggleton P, et al. (2009) Plant traits and wood fates across the globe: rotted, burned, or consumed? Glob Chang Biol 15: 2431–2449. doi: 10.1111/j.1365-2486.2009.01916.x
[2]  Harmon ME, Franklin JF, Swanson FJ, Sollins P, Gregory SV, et al. (1986) Ecology of coarse woody debris in temperate ecosystems. Adv Ecol Res 15: 133–302. doi: 10.1016/s0065-2504(08)60121-x
[3]  Chambers JQ, Higuchi N, Schimel JP, Ferreira LV, Melack JM (2000) Decomposition and carbon cycling of dead trees in tropical forests of the central Amazon. Oecologia 122: 380–388. doi: 10.1007/s004420050044
[4]  Herrmann S, Bauhus J (2013) Effects of moisture, temperature and decomposition stage of respirational carbon loss from coarse woody debris (CWD) of important European tree species. Scand J For Res 28: 346–357. doi: 10.1080/02827581.2012.747622
[5]  Kahl T, Mund M, Bauhus J, Schulze ED (2012) Dissolved organic carbon from European beech logs: Patterns of input to and retention by surface soil. Ecoscience 19: 1–10. doi: 10.2980/19-4-3501
[6]  Litton CM, Raich JW, Ryan MG (2007) Carbon allocation in forest ecosystems. Glob Chang Biol 13: 2089–2109. doi: 10.1111/j.1365-2486.2007.01420.x
[7]  Brunner A, Kimmins JP (2003) Nitrogen fixation in coarse woody debris of Thuja plicata and Tsuga heterophylla forests on northern Vancouver Island. Can J For Res 33: 1670–1682. doi: 10.1139/x03-085
[8]  Lonsdale D, Pautasso M, Holdenrieder O (2008) Wood-decaying fungi in the forest: conservation needs and management options. Eur J For Res 127: 1–22. doi: 10.1007/s10342-007-0182-6
[9]  Rondeux J, Sanchez C (2010) Review of indicators and field methods for monitoring biodiversity within national forest inventories. Core variable: Deadwood. Environ Monit Assess 164: 617–630. doi: 10.1007/s10661-009-0917-6
[10]  Heilmann-Clausen J (2001) A gradient analysis of communities of macrofungi and slime moulds on decaying beech logs. Microbiol Res 105: 575–596. doi: 10.1017/s0953756201003665
[11]  Heilmann-Clausen J, Christensen M (2003) Fungal diversity on decaying beech logs - implications for sustainable forestry. Biodivers Conserv 12: 953–973.
[12]  Müller J, Engel H, Blaschke M (2007) Assemblages of wood-inhabiting fungi related to silvicultural management intensity in beech forests in southern Germany. Eur J For Res 126: 513–527. doi: 10.1007/s10342-007-0173-7
[13]  Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73: 1377–1383. doi: 10.1139/b95-400
[14]  Volkenant K (2007) Totholz als Lebensraum von Mycoz?nosen im fortschreitenden Zersetzungsprozess - Eine Chronosequenzstudie an Fagus sylvatica-Totholz im Nationalpark Kellerwald-Edersee. Berichte des Forschungszentrums Wald?kosysteme: Universit?t Kassel.
[15]  Spano SD, Jurgensen MF, Larsen MJ, Harvey AE (1982) Nitrogen-fixing bacteria in Douglas fir residue decayed by Fomitopsis pinicola. Plant and Soil 68: 117–123. doi: 10.1007/bf02374731
[16]  Blanchette RA (1991) Delignification by wood-decay fungi. Annu Rev Phytopathol 29: 381–398. doi: 10.1146/annurev.py.29.090191.002121
[17]  Cowling EB, Merrill W (1966) Nitrogen in wood and its role in wood deterioration. Can J Bot 44: 1539–1554. doi: 10.1139/b66-167
[18]  Wei?haupt P (2012) Nitrogen uptake of saprotrophic basidiomycetes and bacteria. BAM-Dissertationsreihe ? Band 87: TU Berlin
[19]  Aho PE, Seidler RJ, Evans HJ, Raju PN (1974) Distribution, enumeration, and identification of nitrogen-fixing bacteria associated with decay in living white fir trees. Phytopathology 64: 1413–1420. doi: 10.1094/phyto-64-1413
[20]  Jurgensen MF, Larsen MJ, Spano SD, Harvey AE, Gale MR (1984) Nitrogen-fixation associated with increased wood decay in Douglas fir residue. Forest Science 30: 1038–1044.
[21]  Larsen MJ, Jurgensen MF, Harvey AE, Ward JC (1978) Dinitrogen fixation associated with sporophores of Fomitopsis pinicola, Fomes fomentarius, and Echinodontium tinctorium. Mycologia 70: 1217–1222. doi: 10.2307/3759320
[22]  Seidler RJ, Aho PE, Evans HJ, Raju PN (1972) Nitrogen fixation by bacterial isolates from decay in living white fir trees [Abies concolor (Gord and Glend) Lindl]. J Gen Microbiol 73: 413–&.
[23]  Zehr JP, McReynolds LA (1989) Use of degenerate oligonucleotides for amplification of the Nifh Gene from the marine cyanobacterium Trichodesmium thiebautii. Appl Environ Microbiol 55: 2522–2526.
[24]  Gaby JC, Buckley DH (2011) A global census of nitrogenase diversity. Environ Microbiol 13: 1790–1799. doi: 10.1111/j.1462-2920.2011.02488.x
[25]  Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5: 539–554. doi: 10.1046/j.1462-2920.2003.00451.x
[26]  Wang Q, Quensen JF III, Fish JA, Lee TK, Sun Y, Tiedje JM, Cole JR (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using FrameBot, a new informatics tool. mBio 4(5): e00592–13 doi:10.1128/mBio.00592-13.
[27]  Zhang HB, Yang MX, Tu R (2008) Unexpectedly high bacterial diversity in decaying wood of a conifer as revealed by a molecular method. Int Biodeterior Biodegradation 62: 471–474. doi: 10.1016/j.ibiod.2008.06.001
[28]  Valaskova V, de Boer W, Gunnewiek PJ, Pospisek M, Baldrian P (2009) Phylogenetic composition and properties of bacteria coexisting with the fungus Hypholoma fasciculare in decaying wood. ISME J 3: 1218–1221. doi: 10.1038/ismej.2009.64
[29]  Fischer M, Bossdorf O, Gockel S, Hansel F, Hemp A, et al. (2010) Implementing large-scale and long-term functional biodiversity research: The Biodiversity Exploratories. Basic Appl Ecol 11: 473–485. doi: 10.1016/j.baae.2010.07.009
[30]  Hartigan JA, Wong MA (1979) Algorithm AS 136: A K-means clustering algorithm. J R Stat Soc Ser C Appl Stat 28: 100–108. doi: 10.2307/2346830
[31]  Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19: 11–15.
[32]  Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifh genes in communities of nitrogen fixers in soil. Res Microbiol 152: 95–103. doi: 10.1016/s0923-2508(00)01172-4
[33]  Ramirez-Flandes S, Ulloa O (2008) Bosque: integrated phylogenetic analysis software. Bioinformatics 24: 2539–2541. doi: 10.1093/bioinformatics/btn466
[34]  Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286–298. doi: 10.1093/bib/bbn013
[35]  Kumar S, Skjaeveland A, Orr RJS, Enger P, Ruden T, et al. (2009) AIR: A batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 10: 357. doi: 10.1186/1471-2105-10-357
[36]  Noy NF, Shah NH, Whetzel PL, Dai B, Dorf M, et al. (2009) BioPortal: ontologies and integrated data resources at the click of a mouse. Nucleic Acids Res 37: W170–W173. doi: 10.1093/nar/gkp440
[37]  Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95–98.
[38]  Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194–2200. doi: 10.1093/bioinformatics/btr381
[39]  Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461. doi: 10.1093/bioinformatics/btq461
[40]  Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659. doi: 10.1093/bioinformatics/btl158
[41]  Chien YT, Zinder SH (1996) Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifhDK2) and associated genes in the archaeon Methanosarcina barkeri 227. J Bacteriol 178: 143–148.
[42]  Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541–554.
[43]  Young JPW (2005) The phylogeny and evolution of nitrogenases. In: Palacios R, Newton WE, editors. Genomes and genomics of nitrogen-fixing organisms. Dordrecht: Springer. pp. 221–241.
[44]  Lassmann T, Frings O, Sonnhammer ELL (2009) Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features. Nucleic Acids Res 37: 858–865. doi: 10.1093/nar/gkn1006
[45]  Lassmann T, Sonnhammer ELL (2006) Kalign, Kalignvu and Mumsa: web servers for multiple sequence alignment. Nucleic Acids Res 34: W596–W599. doi: 10.1093/nar/gkl191
[46]  Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132. doi: 10.1016/0022-2836(82)90515-0
[47]  Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14: 1188–1190. doi: 10.1101/gr.849004
[48]  Glez-Pena D, Gomez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Res 38: W14–W18. doi: 10.1093/nar/gkq321
[49]  Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105. doi: 10.1093/bioinformatics/bti263
[50]  Gascuel O (1997) BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685–695. doi: 10.1093/oxfordjournals.molbev.a025808
[51]  Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
[52]  Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286–2288. doi: 10.1093/bioinformatics/btp368
[53]  Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75.
[54]  Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin.
[55]  Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans. pp. 1–8.
[56]  Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. doi: 10.1093/molbev/msr121
[57]  Bouckaert RR (2010) DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26: 1372–1373. doi: 10.1093/bioinformatics/btq110
[58]  Stover BC, Muller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. doi: 10.1186/1471-2105-11-7
[59]  Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267. doi: 10.1093/molbev/msj030
[60]  De'Ath G (2002) Multivariate regression trees: a new technique for modeling species-environment relationships. Ecology 83: 1105–1117. doi: 10.2307/3071917
[61]  Gotelli NJ, Entsminger GL (2009) EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc & Kesey-Bear, Jericho.
[62]  Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85: 74–79. doi: 10.1007/bf00317345
[63]  Ulrich W (2008) Pairs- a FORTRAN program for studying pair wise associations in ecological matrices. www.unitorun.pl/~ulrichw.
[64]  Ulrich W, Zalewski M (2006) Abundance and co-occurrence patterns of core and satellite species of ground beetles on small lake islands. Oikos 114: 338–348. doi: 10.1111/j.2006.0030-1299.14773.x
[65]  Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498–2504. doi: 10.1101/gr.1239303
[66]  Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10: 356. doi: 10.1186/1471-2105-10-356
[67]  Berman-Frank I, Lundgren P, Chen YB, Kupper H, Kolber Z, et al. (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294: 1534–1537. doi: 10.1126/science.1064082
[68]  Silvester WB, Sollins P, Verhoeven T, Cline SP (1982) Nitrogen-fixation and acetylene-reduction in decaying conifer boles - Effects of incubation-time, aeration, and moisture-content. Can J For Res 12: 646–652. doi: 10.1139/x82-098
[69]  Wazny H, Wazny J (1964) über das Auftreten von Spurenelementen im Holz. Holz als Roh- und Werkstoff 22: 299–304. doi: 10.1007/bf02608323
[70]  Hicks WT, Harmon ME, Myrold DD (2003) Substrate controls on nitrogen fixation and respiration in woody debris from the Pacific Northwest, USA. For Ecol Manage 176: 25–35. doi: 10.1016/s0378-1127(02)00229-3
[71]  Shaffer BT, Widmer F, Porteous LA, Seidler RJ (2000) Temporal and spatial distribution of the nifh gene of N2-fixing bacteria in forests and clearcuts in western Oregon. Microb Ecol 39: 12–21. doi: 10.1007/s002489900183
[72]  Fukasawa Y, Osono T, Takeda H (2009) Dynamics of physicochemical properties and occurrence of fungal fruit bodies during decomposition of coarse woody debris of Fagus crenata. J For Res 14: 20–29. doi: 10.1007/s10310-008-0098-0
[73]  Merrill W, Cowling EB (1966) Role of nitrogen in wood deterioration - Amount and distribution of nitrogen in fungi. Phytopathology 56: 1083–1090.
[74]  Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, et al. (2011) Bacterial-fungal interactions: Hyphens between agricultural, clinical, environmental, and food microbiologists Microbiol Mol Biol Rev. 75: 583. doi: 10.1128/mmbr.00020-11
[75]  Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10: 538–550. doi: 10.1038/nrmicro2832
[76]  Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds). Ecol Evol Communities. Cambridge: Harvard University Press. pp. 342–444.
[77]  Horner-Devine MC, Silver JM, Leibold MA, Bohannan BJM, Colwell RK, et al. (2007) A comparison of taxon co-occurrence patterns for macro- and microorganisms. Ecology 88: 1345–1353. doi: 10.1890/06-0286
[78]  Whitaker RJ (2009) Evolution: Spatial scaling of microbial interactions. Current Biology 19: R954–R956. doi: 10.1016/j.cub.2009.09.035
[79]  Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21: 501–507. doi: 10.1016/j.tree.2006.06.012
[80]  Rayner ADM, Boddy L (1988) Fungal communities in the decay of wood. Advances in Microbial Ecology 10: 115–166. doi: 10.1007/978-1-4684-5409-3_4
[81]  Thompson TA, Thorn RG, Smith KT (2012) Hypholoma lateritium isolated from coarse woody debris, the forest floor, and mineral soil in a deciduous forest in New Hampshire. Botany 90: 457–464. doi: 10.1139/b2012-011

Full-Text

comments powered by Disqus