Temporal changes of bacterial communities in the Tuber melanosporum ectomycorrhizosphere during ascocarp development

Mycorrhiza

Volumn 26, Issue 5, 2016, Pages 389-399

  Deveau, Aurélie ^a   Antony Babu, Sanjay ^a,d   Le Tacon, François ^a   Robin, Christophe ^a,c   Frey Klett, Pascale ^a   Uroz, Stéphane ^a,b  

^a UNIVERSITÉ DE LORRAINE   (France)

^b Centre INRA de Nancy   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

16S rRNA based pyrosequencing; Bacterial communities; Ectomycorrhizosphere; Soil ectomycorrhizae interface; Temporal changes; Tuber melanosporum

Indexed keywords

COMMUNITY DYNAMICS; COMMUNITY STRUCTURE; ECTOMYCORRHIZA; FRUITING; FUNGUS; MATURATION; MICROBIAL COMMUNITY; PHENOLOGY; RHIZOSPHERE; RNA; SOIL MICROORGANISM; SPECIES RICHNESS; SYMBIOSIS; TEMPORAL VARIATION;

BACTERIA (MICROORGANISMS); CORYLUS AVELLANA; FUNGI; GAMMAPROTEOBACTERIA; TUBER MELANOSPORUM;

BACTERIAL DNA; FUNGAL DNA;

ASCOMYCETES; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; HAZELNUT; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; TIME FACTOR;

ASCOMYCOTA; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CORYLUS; DNA, BACTERIAL; DNA, FUNGAL; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, FUNGAL; MYCORRHIZAE; PLANT ROOTS; SOIL MICROBIOLOGY; TIME FACTORS;

EID: 84954480523     PISSN: 09406360     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00572-015-0679-7     Document Type: Article

References (60)

1. Antony-Babu S, Murat C, Deveau A et al (2013) An improved method compatible with metagenomic analyses to extract genomic DNA from soils in Tuber melanosporum orchards. J Appl Microbiol 115:163–170
2. Antony-Babu S, Deveau A, Van Nostrand JD et al (2014) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16:2831–2847. doi:10.1111/1462-2920.12294
3. Assigbetse K, Gueye M, Thioulouse J, Duponnois R (2005) Soil bacterial diversity responses to root colonization by an ectomycorrhizal fungus are not root-growth-dependent. Microb Ecol 50:350–359. doi:10.1007/s00248-004-0229-x
4. Barbieri E, Bertini L, Rossi I et al (2005) New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiol Lett 247:23–35
5. Barbieri E, Ceccaroli P, Saltarelli R et al (2010) New evidence for nitrogen fixation within the Italian white truffle Tuber magnatum. Fungal Biol 114:936–942
6. Barke J, Seipke RF, Gruschow S et al (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8:109. doi:10.1186/1741-7007-8-109
7. Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20. doi:10.1016/j.soilbio.2011.09.003
8. Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
9. Burke DJ, Dunham SM, Kretzer AM (2008) Molecular analysis of bacterial communities associated with the roots of Douglas fir (Pseudotsuga menziesii) colonized by different ectomycorrhizal fungi. FEMS Microbiol Ecol 65:299–309
10. Calvaruso C, Turpault MP, Leclerc E et al (2010) Influence of forest trees on the distribution of mineral weathering-associated bacterial communities of the Scleroderma citrinum mycorrhizosphere. Appl Environ Microbiol 76:4780–4787. doi:10.1128/AEM.03040-09
11. Churchland C, Grayston SJ (2014) Specificity of plant-microbe interactions in the tree mycorrhizosphere biome and consequences for soil C cycling. Front Microbiol 5:1–20. doi:10.3389/fmicb.2014.00261
12. Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2006) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240. doi:10.1007/s10533-006-9065-z
13. Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
14. Collignon C, Uroz S, Turpault M-P, Frey-Klett P (2011) Seasons differently impact the structure of mineral weathering bacterial communities in beech and spruce stands. Soil Biol Biochem 43:2012–2022. doi:10.1016/j.soilbio.2011.05.008
15. Courty P-E, Buée M, Diedhiou AG et al (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698
16. Delmont TO, Robe P, Cecillon S et al (2011) Accessing the soil metagenome for studies of microbial diversity. Appl Environ Microbiol 77:1315–1324. doi:10.1128/AEM.01526-10
17. Deveau A, Brulé C, Palin B et al (2010) Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8. Environ Microbiol Rep 2:560–568. doi:10.1111/j.1758-2229.2010.00145.x
18. Epron D, Ngao J, Dannoura M et al (2011) Seasonal variations of belowground carbon transfer assessed by in situ 13 CO 2 pulse labelling of trees. Biogeosciences 8:1153–1168. doi:10.5194/bg-8-1153-2011
19. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
20. Frey-Klett P, Chavatte M, Clausse ML et al (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328
21. Goh C-H, Veliz Vallejos DF, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39:826–839. doi:10.1007/s10886-013-0326-8
22. Gryndler M, Soukupová L, Hršelová H et al (2013) A quest for indigenous truffle helper prokaryotes. Environ Microbiol Rep 5:346–352. doi:10.1111/1758-2229.12014
23. Izumi H, Finlay RD (2011) Ectomycorrhizal roots select distinctive bacterial and ascomycete communities in Swedish subarctic forests. Environ Microbiol 13:819–830. doi:10.1111/j.1462-2920.2010.02393.x
24. Izumi H, Moore E, Killham K et al (2007) Characterisation of endobacterial communities in ectomycorrhizas by DNA- and RNA-based molecular methods. Soil Biol Biochem 39:891–899. doi:10.1016/j.soilbio.2006.10.011
25. Izumi H, Cairney JWG, Killham K et al (2008) Bacteria associated with ectomycorrhizas of slash pine (Pinus elliottii) in south-eastern Queensland, Australia. FEMS Microbiol Lett 282:196–204. doi:10.1111/j.1574-6968.2008.01122.x
26. Kataoka R, Taniguchi T, Ooshima H, Futai K (2008) Comparison of the bacterial communities established on the mycorrhizae formed on Pinus thunbergii root tips by eight species of fungi. Plant Soil 304:267–275. doi:10.1007/s11104-008-9548-x
27. Le Tacon F, Zeller B, Plain C et al (2013) Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique. PLoS One 8:e64626. doi:10.1371/journal.pone.0064626
28. Le Tacon F, Rubini A, Murat C, et al. (2015a) Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.). Ann For Sci. doi: 10.1007/s13595-015-0461-1
29. 13C soil labelling and whole-genome oligoarrays. Plant Soil. doi: 10.1007/s11104-015-2557-7
30. Lebeis SL (2014) The potential for give and take in plant-microbiome relationships. Front Plant Sci 5:287. doi:10.3389/fpls.2014.00287
31. Linderman R (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371
32. López-Mondéjar R, Voříšková J, Větrovský T, Baldrian P (2015) The bacterial community inhabiting temperate deciduous forests is vertically stratified and undergoes seasonal dynamics. Soil Biol Biochem 87:43–50. doi:10.1016/j.soilbio.2015.04.008
33. Martin F, Canet D, Marchal J, Brondeau J (1984) In vivo natural-abundance 13C nuclear magnetic resonance studies of living ectomycorrhizal fungi. Plant Physiol 75:151–153
34. Martin F, Canet D, Marchal J (1985) 13C nuclear magnetic resonance study of mannitol cycle and trehalose synthesis during glucose utilization by the ectomycorrhizal Cenococcum graniforme. Plant Physiol 77:499–502
35. Mello A, Ding GC, Piceno YM et al (2013) Truffle brulés have an impact on the diversity of soil bacterial communities. PLoS One 8(4):e61945. doi:10.1371/journal.pone.0061945
36. Meyer F, Paarmann D, D’Souza M et al (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi:10.1186/1471-2105-9-386
37. Mogge B, Loferer C, Agerer R et al (2000) Bacterial community structure and colonization patterns of Fagus sylvatica L. ectomycorrhizospheres as determined by fluorescence in situ hybridization and confocal laser scanning microscopy. Mycorrhiza 9:271–278. doi:10.1007/PL00009991
38. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266. doi:10.1099/00221287-148-1-257
39. Oksanen J, Blanchet F, Kindt R, et al. (2015) Vegan: Community Ecology Package.
40. On SLW, Atabay HI, Corry JEL et al (1998) Emended description of Campylobacter sputorum and revision of its infrasubspecific (biovar) divisions, including C. sputorum biovar paraureolyticus, a urease-producing variant from cattle and humans. Int J Syst Bacteriol 48:195–206. doi:10.1099/00207713-48-1-195
41. Panke-Buisse K, Poole AC, Goodrich JK et al (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J 9:980–989. doi:10.1038/ismej.2014.196
42. Paolocci F (1999) Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizae. FEMS Microbiol Ecol 28:23–30. doi:10.1016/S0168-6496(98)00088-9
43. Porca E, Jurado V, Žgur-Bertok D et al (2012) Comparative analysis of yellow microbial communities growing on the walls of geographically distinct caves indicates a common core of microorganisms involved in their formation. FEMS Microbiol Ecol 81:255–266. doi:10.1111/j.1574-6941.2012.01383.x
44. Rädecker N, Pogoreutz C, Voolstra CR et al (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23:490–497. doi:10.1016/j.tim.2015.03.008
45. Rambelli A (1973) The rhizosphere of mycorrhizae. In: Marks G, Kozlowski T (eds) Ectomycorrhizae their Ecol. Physiol. Academic Press, New York, pp 299–343
46. Rasche F, Knapp D, Kaiser C et al (2011) Seasonality and resource availability control bacterial and archaeal communities in soils of a temperate beech forest. ISME J 5:389–402. doi:10.1038/ismej.2010.138
47. Sbrana C, Agnolucci M, Bedini S et al (2002) Diversity of culturable bacterial populations associated to Tuber borchii ectomycorrhizas and their activity on T. borchii mycelial growth. FEMS Microbiol Lett 211:195–201. doi:10.1016/S0378-1097(02)00712-7
48. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09
49. Schoenian I, Spiteller M, Ghaste M et al (2011) Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci U S A 108:1955–1960. doi:10.1073/pnas.1008441108
50. Schommer NN, Gallo RL (2013) Structure and function of the human skin microbiome. Trends Microbiol 21:660–668. doi:10.1016/j.tim.2013.10.001
51. Shafquat A, Joice R, Simmons SL, Huttenhower C (2014) Functional and phylogenetic assembly of microbial communities in the human microbiome. Trends Microbiol 22:261–266. doi:10.1016/j.tim.2014.01.011
52. Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
53. Stomeo F, Portillo MC, Gonzalez JM et al (2008) Pseudonocardia in white colonizations in two caves with Paleolithic paintings. Int Biodeterior Biodegrad 62:483–486. doi:10.1016/j.ibiod.2007.12.011
54. Stres B, Danevcic T, Pal L et al (2008) Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiol Ecol 66:110–122. doi:10.1111/j.1574-6941.2008.00555.x
55. Tabuchi H, Kato K, Nioh I (2008) Season and soil management affect soil microbial communities estimated using phospholipid fatty acid analysis in a continuous cabbage (Brassica oleracea var. capitata) cropping system. Soil Sci Plant Nutr 54:369–378. doi:10.1111/j.1747-0765.2008.00242.x
56. Uroz S, Calvaruso C, Turpault MP et al (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027. doi:10.1128/AEM.00121-07
57. Uroz S, Oger P, Morin E, Frey-Klett P (2012) Distinct ectomycorrhizospheres share similar bacterial communities as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 78:3020–3024. doi:10.1128/AEM.06742-11
58. Uroz S, Courty PE, Pierrat JC et al (2013) Functional profiling and distribution of the forest soil bacterial communities along the soil mycorrhizosphere continuum. Microb Ecol 66:404–415. doi:10.1007/s00248-013-0199-y
59. Vik U, Logares R, Blaalid R et al (2013) Different bacterial communities in ectomycorrhizae and surrounding soil. Sci Rep 3:3471. doi:10.1038/srep03471
60. Yano JM, Yu K, Donaldson GP et al (2015) Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 161:264–276. doi:10.1016/j.cell.2015.02.047