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Metagenomics of Plant Microbiomes

  • G. BraderEmail author
  • E. Corretto
  • A. Sessitsch

Abstract

The collective genomes of the holobiont plant comprising diverse microbiota encode a number of functions required for the host as well as for supporting the interaction between the plant and its associated microbiome. This chapter reviews various plant habitats for microorganisms, microbiome functions, and functional as well as sequence-based metagenomics screening approaches, which can be used to elucidate holobiont functioning.

References

  1. Abbà S, Galetto L, Carle P et al (2014) RNA-Seq profile of flavescence dorée phytoplasma in grapevine. BMC Genomics 15:1088PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adams IP, Glover RH, Monger WA et al (2009) Next-generation sequencing and metagenomic analysis: a universal diagnostic tool in plant virology. Mol Plant Pathol 104:5375–5345Google Scholar
  3. Alvarez TM, Goldbeck R, Santos CR et al (2013a) Development and biotechnological application of a novel endoxylanase family GH10 identified from sugarcane soil metagenome. PLoS One 8:e70014PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alvarez TM, Paiva JH, Ruiz DM et al (2013b) Structure and function of a novel cellulase 5 from sugarcane soil metagenome. PLoS One 8:e83635PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bag S, Al Rwahnih M, Li A et al (2015) Detection of a new luteovirus in imported nectarine trees: a case study to propose adoption of metagenomics in post-entry quarantine. Phytopathology 105:840–846PubMedCrossRefGoogle Scholar
  6. Bai Y, Liang J, Liu R et al (2014) Metagenomic analysis reveals microbial diversity and function in the rhizosphere soil of a constructed wetland. Environ Technol 35:2521–2527PubMedCrossRefGoogle Scholar
  7. Bai Y, Müller DB, Srinivas G et al (2015) Functional overlap of the Arabidopsis leaf and root microbiota. Nature 528:364–369PubMedCrossRefGoogle Scholar
  8. Barry SM, Challis GL (2009) Recent advances in siderophore biosynthesis. Curr Opin Chem Biol 13:205–215PubMedCrossRefGoogle Scholar
  9. Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486PubMedCrossRefGoogle Scholar
  10. Bertaccini A, Duduk B, Paltrinieri S, Contaldo N (2014) Phytoplasmas and Phytoplasma diseases: a severe threat to agriculture. Am J Plant Sci 5:1763–1788CrossRefGoogle Scholar
  11. Besserer A, Puech-Pages V, Kiefer P et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226PubMedPubMedCentralCrossRefGoogle Scholar
  12. Blainey PC (2013) The future is now: single-cell genomics of bacteria and archaea. FEMS Microbiol Rev 37:407PubMedCrossRefGoogle Scholar
  13. Bordenstein SR, Theis KR (2015) Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol 13:e1002226PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bragina A, Maier S, Berg C et al (2012) Similar diversity of alphaproteobacteria and nitrogenase gene amplicons on two related Sphagnum mosses. Front Microbiol 2:275PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bragina A, Berg C, Müller H (2013) Insights into functional bacterial diversity and its effect on Alpine bog ecosystem functioning. Sci Rep 3:1955PubMedCrossRefGoogle Scholar
  16. Bragina A, Oberauner-Wappis L, Zachow C et al (2014) The Sphagnum microbiome supports ecosystem functioning under extreme conditions. Mol Ecol 23:4498–4510PubMedCrossRefGoogle Scholar
  17. Bragina A, Berg C, Berg G (2015) The core microbiome bonds the Alpine bog vegetation to a transkingdom metacommunity. Mol Ecol 24:4795–4807PubMedCrossRefGoogle Scholar
  18. Buee M, De Boer W, Martin F, van Overbeek L, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212CrossRefGoogle Scholar
  19. Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95PubMedCrossRefGoogle Scholar
  20. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838PubMedCrossRefGoogle Scholar
  21. Bulgarelli D, Garrido-Oter R, Münch PC et al (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bush LP, Wilkinson HH, Schardl CL (1997) Bioprotective alkaloids of grass-fungal endophyte symbioses. Plant Physiol 114:1–7PubMedPubMedCentralCrossRefGoogle Scholar
  23. Calheiros CSC, Duque AF, Moura A et al (2009) Substrate effect on bacterial communities from constructed wetlands planted with Typha latifolia treating industrial wastewater. Ecol Eng 35:744–753CrossRefGoogle Scholar
  24. Camerota C, Raddadi N, Pizzinat A et al (2012) Incidence of ‘Candidatus Liberibacter europaeus’ and phytoplasmas in Cacopsylla species (Hemiptera: Psyllidae) and their host/shelter plants. Phytoparasitica 40:213–221CrossRefGoogle Scholar
  25. Caporaso JG, Lauber CL, Walters WA et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624PubMedPubMedCentralCrossRefGoogle Scholar
  26. Carlier AL, Eberl L (2012) The eroded genome of a Psychotria leaf symbiont: hypotheses about lifestyle and interactions with its plant host. Environ Microbiol 14:2757–2769PubMedCrossRefGoogle Scholar
  27. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803PubMedCrossRefGoogle Scholar
  28. Charlop-Powers Z, Owen J, Reddy B et al (2015) Global biogeographic sampling of bacterial secondary metabolism. elife 4:e05048PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cheng J, Pinnell L, Engel K, Neufeld JD, Charles TC (2014) Versatile broad-host-range cosmids for construction of high quality metagenomic libraries. J Microbiol Method 99:27–34CrossRefGoogle Scholar
  30. Chhabra S, Brazil D, Morrissey J et al (2013) Characterization of mineral phosphate solubilization traits from a barley rhizosphere soil functional metagenome. Microbiol Open 2:717–724Google Scholar
  31. Cobo-Díaz JF, Fernández-González AJ, Villadas PJ et al (2015) Metagenomic assessment of the potential microbial nitrogen pathways in the rhizosphere of a Mediterranean forest after a wildfire. Microb Ecol 69:895–904PubMedCrossRefGoogle Scholar
  32. Compant S, Cement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  33. Cretiou MS, Kielak AM, Abu Al-Soud W et al (2012) Mining of unexplored habitats for novel chitinases – chiA as a helper gene proxy in metagenomics. Appl Microbiol Biotechnol 94(5):1347–1358CrossRefGoogle Scholar
  34. Duan YP, Zhou LJ, Hall DG et al (2009) Complete genome sequence of citrus Huanglongbing bacterium, ‘Candidatus Liberibacter asiaticus’ obtained through metagenomics. Mol Plant-Microbe Interact 22:1011–1020PubMedCrossRefGoogle Scholar
  35. Engel K, Pinnell L, Cheng J, Charles TC, Neufeld JD (2012) Nonlinear electrophoresis for purification of soil DNA for metagenomics. J Microbiol Method 88:35–40CrossRefGoogle Scholar
  36. Engel K, Ashby D, Brady SF et al (2013) Meeting report: 1st international functional metagenomics workshop May 7-8, 2012, St Jacobs, Ontario, Canada. Stand Genom Sci 8(1):106–111CrossRefGoogle Scholar
  37. Erlacher A, Cernava T, Cardinale M et al (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6:53PubMedPubMedCentralCrossRefGoogle Scholar
  38. Escobar MA, Dandekar AM (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 8:380–386PubMedCrossRefGoogle Scholar
  39. Fibach-Baldi S, Burdman S, Okon Y (2012) Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. FEMS Microbiol Lett 326:99–108CrossRefGoogle Scholar
  40. Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468PubMedCrossRefGoogle Scholar
  41. Gilbert J, Li LL, Taghavi S et al (2012) Bioprospecting metagenomics for new glycoside hydrolases. Methods Mol Biol 908:141–151PubMedCrossRefGoogle Scholar
  42. Grube M, Cernava T, Soh J et al (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative genomics. ISME J 9:412–424PubMedCrossRefGoogle Scholar
  43. Guerriero G, Hausman JF, Strauss J et al (2015) Destructuring plant biomass: focus on fungal and extremophilic cell wall hydrolases. Plant Sci 234:180–193PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hoshi A, Oshima K, Kakizawa S et al (2009) A unique virulence factor for proliferation and dwarfism in plants identified from a phytopathogenic bacterium. Proc Natl Acad Sci U S A 106:6416–6421PubMedPubMedCentralCrossRefGoogle Scholar
  46. Imfeld G, Aragones CE, Fetzer I et al (2010) Characterization of microbial communities in the aqueous phase of a constructed model wetland treating 1,2-dichloroethene-contaminated groundwater. FEMS Microbiol Ecol 72:74–88PubMedCrossRefGoogle Scholar
  47. Junker R, Loewel C, Gross R et al (2011) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918PubMedCrossRefGoogle Scholar
  48. Kakizawa S, Makino A, Ishii Y et al (2014) Draft genome sequence of “Candidatus Phytoplasma asteris” strain OY-V, an unculturable plant-pathogenic bacterium. Genome Announc 18:2Google Scholar
  49. Lebeis SL (2015) Greater than the sum of their parts: characterizing plant microbiomes at the community level. Curr Opin Plant Biol 24:82–86PubMedCrossRefGoogle Scholar
  50. Lee SW, Kim HK, Lim HK et al (2004) Searching antimicrobial activities from plant rhizosphere metagenomics library. Phytopathology 94:S59Google Scholar
  51. Lee MH, Hong KS, Malhotra S et al (2010) A new esterase EstD2 isolated from plant rhizosphere soil metagenome. Appl Microbiol Biotechnol 88:1125–1134PubMedCrossRefGoogle Scholar
  52. Lee S, Ishiga Y, Clermont K, Mysore KS (2013) Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by non-host bacterial pathogens. PeerJ 1:e34PubMedPubMedCentralCrossRefGoogle Scholar
  53. Leininger S, Urich T, Schloter M et al (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809PubMedCrossRefGoogle Scholar
  54. Lin H, Lou B, Glynn JM et al (2011) The complete genome sequence of ‘Candidatus Liberibacter solanacearum’, the bacterium associated with potato zebra chip disease. PLoS One 6(4):e19135PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490PubMedCrossRefGoogle Scholar
  56. Lundberg DS, Lebeis SL, Paredes SH (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90PubMedPubMedCentralCrossRefGoogle Scholar
  57. Martin M, Biver S, Barbeyron T et al (2014) identification and characterization of a halotolerant, cold-active marine endo-ß-1,4-glucanase by using functional metagenomics of seaweed-associated microbiota. Appl Environ Microbiol 80:4958–4967PubMedPubMedCentralCrossRefGoogle Scholar
  58. Mason CJ, Couture JJ, Raffa KF (2014) Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 175:901–910PubMedCrossRefGoogle Scholar
  59. McCormick SP (2013) Microbial detoxification of mycotoxins. J Chem Ecol 39:907–918PubMedCrossRefGoogle Scholar
  60. Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663PubMedCrossRefGoogle Scholar
  61. Mitrovic J, Siewert C, Duduk B et al (2014) Generation and analysis of draft sequences of ‘Stolbur’ Phytoplasma from multiple displacement amplification templates. J Mol Microbiol Biotechnol 24:1–11PubMedCrossRefGoogle Scholar
  62. Mitter B, Petric A, Shin MW et al (2013a) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120PubMedPubMedCentralCrossRefGoogle Scholar
  63. Mitter B, Brader G, Afzal M et al (2013b) Advances in elucidating plant-soil-microbe (bacteria) interactions. Adv Agronomy 121:381–445CrossRefGoogle Scholar
  64. Morohoshi T, Oikawa M, Sato S et al (2011) Isolation and characterization of novel lipases from a metagenomic library of the microbial community in the pitcher fluid of the carnivorous plant Nepenthes hybrida. J Biosci Bioeng 112:315–320PubMedCrossRefGoogle Scholar
  65. Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14:557–562PubMedCrossRefGoogle Scholar
  66. Neufeld J, Engel K, Cheng J et al (2011) Open resource metagenomics: a model for sharing metagenomic libraries. Stand Genom Sci 5(2):203–210CrossRefGoogle Scholar
  67. Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676PubMedCrossRefGoogle Scholar
  68. Ofek-Lalzar M, Sela N, Goldman-Voronov M et al (2014) Niche and host-associated functional signatures of the root surface microbiome. Nat Commun 5:4950PubMedCrossRefGoogle Scholar
  69. Osbourn AE, Qi X, Townsend B, Qin B (2003) Dissecting plant secondary metabolism - constitutive chemical defenses in cereals. New Phytol 159:101–108CrossRefGoogle Scholar
  70. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefGoogle Scholar
  71. Peiffer JA, Spor A, Koren O et al (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110:6548–6553PubMedPubMedCentralCrossRefGoogle Scholar
  72. Porazinska DL, Morgan MJ, Gaspar JM et al (2014) Discrimination of plant-parasitic nematodes from complex soil communities using ecometagenetics. Phytopathology 104:749–761PubMedCrossRefGoogle Scholar
  73. Puspita ID, Kamagata Y, Tanaka M, Asano K, Nakatsu CH (2012) Are uncultivated bacteria really uncultivable? Microbes Environ 27:356–366PubMedPubMedCentralCrossRefGoogle Scholar
  74. Raaijmakers JM, Mazzola M (2012) Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu Rev Phytopathol 50:403–424PubMedCrossRefGoogle Scholar
  75. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037PubMedCrossRefGoogle Scholar
  76. Ramirez-Puebla ST, Servin-Garciduenas LE, Jimenez-Marin B et al (2013) Gut and root microbiota commonalities. Appl Environ Microbiol 79:2–9PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rasche F, Hödl V, Poll C et al (2006a) Rhizosphere bacteria affected by transgenic potatoes with antibacterial activities in comparison to effects of soil, wildtype potatoes, vegetation stage and pathogen exposure. FEMS Microbiol Ecol 56:219–235PubMedCrossRefGoogle Scholar
  78. Rasche F, Velvis H, Zachow C et al (2006b) Impact of transgenic potatoes expressing antibacterial agents on bacterial endophytes is comparable to effects of wildtype potatoes and changing environmental conditions. J Appl Ecol 43:555–566CrossRefGoogle Scholar
  79. Rastogi G, Coaker GL, Leveau JHJ (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348:1–10PubMedCrossRefGoogle Scholar
  80. Roossinck MJ, Martin DP, Roumagnac P (2015) Plant virus metagenomics: advances in virus discovery. Phytopathology 105:716–727PubMedCrossRefGoogle Scholar
  81. Rosenberg E, Sharon G, Zilber-Rosenberg I (2009) The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol 11:2959–2962PubMedCrossRefGoogle Scholar
  82. Ryan RP, Monchy S, Cardinale M et al (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525PubMedCrossRefGoogle Scholar
  83. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340PubMedCrossRefGoogle Scholar
  84. Sessitsch A, Hardoim P, Döring J et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microb Interact 25:28–36CrossRefGoogle Scholar
  85. Siewert C, Luge T, Duduk B et al (2014) Analysis of expressed genes of the bacterium Candidatus Phytoplasma Mali: highlights key features of virulence and metabolism. PLoS One 9:e94391PubMedPubMedCentralCrossRefGoogle Scholar
  86. Singh S (2014) A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J Appl Microbiol 117:1221–1244PubMedCrossRefGoogle Scholar
  87. Singh A, Sarma BK, Harikesh B, Upadhyay RS (2014) Trichoderma: a silent worker of plant rhizosphere. In: Gupta VK, Schmoll M, Herrera-Estrella A, Upadhyay RS, Druzhinina I, Ruohy MG (eds) Biotechnology and biology of Trichoderma. Elsevier, The Netherlands, pp 533–542CrossRefGoogle Scholar
  88. Singh RP, Kumari P, Reddy CRK (2015) Antimicrobial compounds from seaweeds-associated bacteria and fungi. Appl Microbiol Biotechnol 99:1571–1586PubMedCrossRefGoogle Scholar
  89. Souza RC, Cantão ME, Ribeiro Vasconcelos AT et al (2013) Soil metagenomics reveals differences under conventional and no-tillage with crop rotation or succession. Appl Soil Ecol 72:49–61CrossRefGoogle Scholar
  90. Stottmeister U, Wissner A, Kuschk P et al (2003) Effects of plants and microorganisms in constructed wetlands for wastewater treatment. Biotechnol Adv 22:93–117PubMedCrossRefGoogle Scholar
  91. Suzaki T, Ito M, Kawaguchi M (2013) Genetic basis of cytokinin and auxin functions during root nodule development. Front Plant Science 4:42CrossRefGoogle Scholar
  92. Swain SM, Singh DP (2005) Tall tales from sly dwarves: novel functions of gibberellins in plant development. Trends Plant Sci 10:123–129PubMedCrossRefGoogle Scholar
  93. Toth IK, Bell KS, Holeva MC, Birch PR (2003) Soft rot Erwiniae: from genes to genomes. Mol Plant Pathol 4:17–30PubMedCrossRefGoogle Scholar
  94. Tsurumaru H, Okubo T, Okazaki K et al (2015) Metagenomic analysis of the bacterial community associated with the taproot of sugar beet. Microbes Environ 30:63–69PubMedPubMedCentralCrossRefGoogle Scholar
  95. Turner TR, Ramakrishnan K, Walshaw J et al (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258PubMedPubMedCentralCrossRefGoogle Scholar
  96. Vacheron J, Desbrosses G, Bouffaud M-L et al (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356PubMedPubMedCentralCrossRefGoogle Scholar
  97. Vadassery J, Ritter C, Venus Y et al (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica. Mol Plant-Microbe Interact 21:1371–1383PubMedCrossRefGoogle Scholar
  98. Verastegui Y, Cheng J, Engel K et al (2014) Multisubstrate isotope labeling and metagenomic analysis of active soil bacterial communities. MBio 5:e01157-14PubMedPubMedCentralCrossRefGoogle Scholar
  99. Vey G, Charles TC (2014). MetaProx: the database of metagenomic proximons. Database 2014:ID bau097Google Scholar
  100. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840PubMedCrossRefGoogle Scholar
  101. Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209PubMedCrossRefGoogle Scholar
  102. Weinert N, Piceno Y, Ding GC et al (2011) PhyloChip hybridization uncovered an enormous bacterial diversity in the rhizosphere of different potato cultivars: many common and few cultivar-dependent taxa. FEMS Microbiol Ecol 75:497–506PubMedCrossRefGoogle Scholar
  103. Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci U S A 98:3889–3894PubMedPubMedCentralCrossRefGoogle Scholar
  104. Yilmaz S, Singh AK (2012) Single cell genome sequencing. Curr Opin Biotechnol 23:437–443PubMedCrossRefGoogle Scholar
  105. Zarraonaindia I, Owens SM, Weisenhorn P et al (2015) The soil microbiome influences grapevine-associated microbiota. MBio 6:e02527-14PubMedPubMedCentralCrossRefGoogle Scholar
  106. Zuccaro A, Schoch CL, Spatafora JW et al (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol 74:931–941PubMedCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Center for Health and BioresourcesAIT Austrian Institute of Technology GmbH, Bioresources UnitTullnAustria

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