Deciphering the presence and activity of fungal communities in marine sediments using a model estuarine system

Aquatic Microbial Ecology

Volumn 70, Issue 1, 2013, Pages 45-62

  Burgaud, Gaëtan ^a   Woehlke, Sarah ^b   Rédou, Vanessa ^a   Orsi, William ^a   Beaudoin, David ^a   Barbier, Georges ^a   Biddle, Jennifer F ^b   Edgcomb, Virginia P ^a  

^a UNIVERSITÉ DE BREST   (France)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

cDNA; Cultivation; Delaware Bay; DNA; Fungi; Subsurface sediments

Indexed keywords

EID: 84880020106     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01638     Document Type: Article

References (100)

1. Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin. Environ Microbiol 11: 360-381
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
3. Amann RI, Ludwig W, Schleifer K (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169
4. Arhipova N, Gaitnieks T, Donis J, Stenlid J, Vasaitis R (2011) Decay, yield loss and associated fungi in stands of grey alder (Alnus incana) in Latvia. Forestry 84: 337-348
5. Arzanlou M, Groenewald JZ, Gams W, Braun U, Shin HD, Crous PW (2007) Phylogenetic and morphotaxonomic revision of Ramichloridium and allied genera. Stud Mycol 58: 57-93
6. Bass D, Howe A, Brown N, Barton H and others (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc R Soc Lond B Biol Sci 274: 3069-3077
7. Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10: 189
8. Belliveau MJ, Bärlocher F (2005) Molecular evidence confirms multiple origins of aquatic hyphomycetes. Mycol Res 109: 1407-1417
9. Biddle JF, House CH, Brenchley JE (2005) Microbial stratification in deeply buried marine sediment reflects changes in sulfate/methane profiles. Geobiology 3: 287-295
10. Biddle JF, Fitz-Gibbon S, Schuster SC, Brenchley JE, House CH (2008) Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci USA 105: 10583-10588
11. Blanchette RA, Held BW, Jurgens JA, McNew DL, Harrington TC, Duncan SM, Farrell RL (2004) Wood-destroying soft rot fungi in the historic expedition huts of Antarctica. Appl Environ Microbiol 70: 1328-1335
12. Bodensteiner P, Binder M, Moncalvo JM, Agerer R, Hibbett DS (2004) Phylogenetic relationships of cyphelloid homobasidiomycetes. Mol Phylogenet Evol 33: 501-515
13. Branda E, Turchetti B, Diolaiuti G, Pecci M, Smiraglia C & Buzzini P (2010) Yeast and yeast-like diversity in the southernmost glacier of Europe (Calderone Glacier, Apennines, Italy). FEMS Microbiol Ecol 72:354-369
14. Burgaud G, Le Calvez T, Arzur D, Vandenkoornhuyse P, Barbier G (2009) Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol 11: 1588-1600
15. Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol Ecol 73: 121-133
16. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K and others (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336
17. Cathrine SJ, Raghukumar C (2009) Anaerobic denitrification in fungi from the coastal marine sediments off Goa, India. Mycol Res 113: 100-109
18. Chaverri P, Gazis RO (2011) Linking ex planta fungi with their endophytic stages: Perisporiopsis, a common leaf litter and soil fungus, is a frequent endophyte of Hevea spp. and other plants. Fungal Ecol 4: 94-102
19. Coelho MA, Gonçalves P, Sampaio JP (2011) Evidence for maintenance of sex determinants but not of sexual stages in red yeasts, a group of early diverged basidiomyctes. BMC Evol Biol 11: 249
20. Cole JR, Chai B, Marsh TL, Farris RJ and others (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31: 442-443
21. Cordier T, Robin C, Capdevielle X, Fabreguettes O, Desprez-Loustau ML, Vacher C (2012) The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica) varies significantly along an elevation gradient. New Phytol 196:510-519
22. Cueva C, García-Ruiz A, González-Rompinelli E, Bartolome B and others (2012) Degradation of biogenic amines by vineyard ecosystem fungi. Potential use in winemaking. J Appl Microbiol 112: 672-682
23. Damare S, Raghukumar C (2008) Fungi and macroaggregation in deep-sea sediments. Microb Ecol 56: 168-177
24. Damare S, Raghukumar C, Raghukumar S (2006) Fungi in deep-sea sediments of the Central Indian Basin. Deep-Sea Res I 53: 14-27
25. Diener A (2012) Visualizing and quantifying Fusarium oxysporum in the plant host. Mol Plant Microbe Interact 25: 1531-1541
26. Edgcomb VP, Biddle JF (2012) Microbial eukaryotes in the marine subsurface? In: Altenbach AV, Bernhard JM, Seckbach J (eds) Anoxia: Evidence for eukaryote survival and paleontological strategies. Springer, Dordrecht, p 479-493
27. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci USA 99: 7658-7662
28. Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13: 172-183
29. Ellouze W, Hamel C, Vujanovic V, Gan Y, Bouzid S, St-Arnaud M (2013) Chickpea genotypes shape the soil microbiome and affect the establishment of the subsequent durum wheat crop in the semiarid North American Great Plains. Soil Biol Biochem 63:129-141
30. Fasanella CC, Dias ACF, Rigonato J, Fiore MF and others (2012) The selection exerted by oil contamination on mangrove fungal communities. Water Air Soil Pollut 223: 4233-4243
31. Fernandes PMB, Domitrovic T, Kao CM, Kurtenbach E (2004) Genomic expression pattern in Saccharomyces cerevisiae cells in response to high hydrostatic pressure. FEBS Lett 556: 153-160
32. Flowers J, Hartman J, Vaillancourt L (2003) Detection of latent Sphaeropsis sapinea infections in Austrian pine tissues using nested-polymerase chain reaction. Phytopathology 93: 1471-1477
33. Gadanho M, Sampaio JP (2005) Occurrence and diversity of yeasts in the Mid-Atlantic Ridge hydrothermal fields near the Azores Archipelago. Microb Ecol 50: 408-417
34. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111: 3-49
35. Gao Y, Zhao JT, Zu YG, Fu YJ, Wang W, Luo M, Efferth T (2011) Characterization of five fungal endophytes producing Cajaninstilbene acid isolated from pigeon pea [Cajanus cajan (L.) Millsp]. PLoS ONE 6: e27589
36. Gazis R, Chaverri P (2010) Diversity of fungal endophytes in leaves and stems of wild rubber trees (Hevea brasiliensis) in Peru. Fungal Ecol 3: 240-254
37. Gonçalves VN, Vaz AB, Rosa CA, Rosa LH (2012) Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol Ecol 82: 459-471
38. Gorfer M, Blumhoff M, Klaubauf S, Urban A and others (2011) Community profiling and gene expression of fungal assimilatory nitrate reductases in agricultural soil. ISME J 5: 1771-1783
39. Grubisic LM, Brutemark A, Weyhenmeyer GA, Wikner J, Båmstedt U, Bertillson S (2012) Effects of stratification depth and dissolved organic matter on brackish bacterioplankton communities. Mar Ecol Prog Ser 453: 37-48
40. Gutiérrez MH, Pantoja S, Tejoset E, Quinones RA (2011) The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar Biol 158: 205-219
41. Hawksworth DL (2009) Mycology: a neglected megascience. In: Rai M, Bridge PD (eds) Applied mycology. CABI Publishing, Wallingford, p 1-16
42. House C, Cragg B, Teske A (2003) Drilling contamination tests on ODP leg 201 using chemical and particulate tracers. Proceedings of the Ocean Drilling Program, initial reports 201. Ocean Drilling Program, Texas A&M University, College Station, TX
43. Jebaraj CS, Raghukumar C, Behnke A, Stoeck T (2010) Fungal diversity in oxygen-depleted regions of the Arabian Sea revealed by targeted environmental sequencing combined with cultivation. FEMS Microbiol Ecol 71: 399-412
44. Jumpponen A, Jones KL (2009) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol 184: 438-448
45. Kallmeyer J, Smith DC, Spivack AJ, D'Hondt S (2008) New cell extraction procedure applied to deep subsurface sediments. Limnol Oceanogr Methods 6: 236-245
46. Kallmeyer J, Pockalny R, D'Hondt S (2009) Quantifying global subseafloor microbial abundance: method and implications. Goldschmidt Conference Abstracts 2009. Geochim Cosmochim Acta 73(13): Suppl 615
47. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D'Hondt S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci USA 109: 16213-16216
48. Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic Press, London
49. Krüger M, Stockinger H, Krüger C, Schüssler A (2009) DNAbased species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183: 212-223
50. Lai X, Cao L, Tan H, Fang S, Huang Y, Zhou S (2007) Fungal communities from methane hydrate-bearing deep-sea marine sediments in South China Sea. ISME J 1: 756-762
51. Le Calvez T, Burgaud G, Mahe S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep sea hydrothermal ecosystems. Appl Environ Microbiol 75: 6415-6421
52. Letcher PM, Powell MJ, Churchill PF, Chambers JG (2006) Ultrastructural and molecular phylogenetic delineation of a new order, the Rhizophydiales (Chytridiomycota). Mycol Res 110: 898-915
53. López-García P, Philippe H, Gail F, Moreira D (2003) Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci USA 100: 697-702
54. López-García P, Vereshchaka A, Moreira D (2007) Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost City hydrothermal field. Environ Microbiol 9: 546-554
55. Madrid H, Cano J, Stchigel A, Gené J, Guarro J (2010) Ramophialophora humicola and Fibulochlamys chilensis, two new microfungi from soil. Mycologia 102: 605-612
56. Marincowitz S, Crous PW, Groenewald JZ, Wingfield MJ (2008) Microfungi occurring on Proteaceae in the fynbos. CBS Biodiversity Series, Vol 7. CBS-KNAW Fungal Biodiversity Centre, Utrecht
57. Mohamed DJ, Martiny JBH (2011) Patterns of fungal diversity and composition along a salinity gradient. ISME J 5: 379-388
58. Monchy S, Sanciu G, Jobard M, Rasconi S and others (2011) Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environ Microbiol 13: 1433-1453
59. Morales VM, Jasalavich CA, Pelcher LE, Petrie GA, Taylor JL (1995) Phylogenetic relationship among several Leptosphaeria species based on their ribosomal DNA sequences. Mycol Res 99: 593-603
60. Mouton M, Postma F, Wilsenach J, Botha A (2012) Diversity and characterization of culturable fungi from marine sediment collected from St. Helena Bay, South Africa. Microb Ecol 64: 311-319
61. Nagahama T, Hamamoto M, Nakase T, Horikoshi K (1999) Kluyveromyces nonfermentans sp. nov., a new yeast species isolated from the deep sea. Int J Syst Bacteriol 49: 1899-1905
62. Nagahama T, Hamamoto M, Nakase T, Takami H, Horikoshi K (2001) Distribution and identification of red yeasts in deep-sea environments around the northwest Pacific Ocean. Antonie van Leeuwenhoek 80: 101-110
63. Nagahama T, Hamamoto M, Nakase T, Takaki Y, Horikoshi K (2003) Cryptococcus surugaensis sp. nov., a novel yeast species from sediment collected on the deep-sea floor of Suruga Bay. Int J Syst Evol Microbiol 53: 2095-2098
64. Nagahama T, Hamamoto M, Horikoshi K (2006) Rho dotorula pacifica sp. nov., a novel yeast species from sediment collected on the deep-sea floor of the north-west Pacific Ocean. Int J Syst Evol Microbiol 56: 295-299
65. Nagahama T, Abdel-Wahab MA, Nogi Y, Miyazaki M, Uematsu K, Hamamoto M, Horikoshi K (2008) Dipodascus tetrasporeus sp. nov., an ascosporogenous yeast isolated from deep-sea sediments in the Japan Trench. Int J Syst Evol Microbiol 58: 1040-1046
66. Nagano Y, Nagahama T, Hatada Y, Nunoura T and others (2010) Fungal diversity in deep-sea sediments-the presence of novel fungal groups. Fungal Ecol 3: 316-325
67. Oger PM, Jebbar M (2010) The many ways of coping with pressure. Res Microbiol 161: 799-809
68. Osono T, Takeda H (2007) Microfungi associated with Abies needles and Betula leaf litter in a subalpine coniferous forest. Can J Microbiol 53: 1-7
69. Paradi I, Baar J (2007) Mycorrhizal fungal diversity in willow forests of different age along the river Waal, The Netherlands. For Ecol Manage 237: 366-372
70. Pedras MS, Sarma-Mamillapalle V (2012) Metabolism and metabolites of dithiocarbamates in the plant pathogenic fungus Leptosphaeria maculans. J Agric Food Chem 60: 7792-7798
71. Pernthaler J, Glöckner FO, Schönhuber W, Amann R (2001) Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol 30: 207-210
72. Persson Y, Vasaitis R, Långström B, Ohrn P, Ihrmark K, Stenlid J (2009) Fungi vectored by the bark beetle Ips typographus following hibernation under the bark of standing trees and in the forest litter. Microb Ecol 58: 651-659
73. Pindi PK (2012) Diversity of fungi at various depths of marine water. Res Biotechnol 3: 62-66
74. Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818
75. Raghukumar C, Raghukumar S, Sheelu G, Gupta SM, Nagender Nath B, Rao BR (2004) Buried in time: culturable fungi in a deep-sea sediment core from the Chagos Trench, Indian Ocean. Deep-Sea Res I 51: 1759-1768
76. Richards TA, Jones MD, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci 4: 495-522
77. Rodrigues A, Mueller UG, Ishak HD, Bacci M Jr, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78: 244-255
78. Santoro EB (2004) Delaware estuary monitoring report. Delaware River Basin Commission, West Trenton, NJ
79. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, and Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109: 6241-6246
80. Scorzetti G, Fell JW, Fonseca A, Statzell-Tallman A (2002) Systematics of basidiomycetous yeasts: a comparison of large subunit D1/D2 and internal transcribed spacer rDNA regions. FEMS Yeast Res 2: 495-517
81. Shrestha P, Szaro TM, Bruns TD, Taylor JW (2011) Systematic search for cultivatable fungi that best deconstruct cell walls of Miscanthus and sugarcane in the field. Appl Environ Microbiol 77: 5490-5504
82. Singh P, Raghukumar C, Vermaet P, Shouche Y (2010) Phylogenetic diversity of culturable fungi from the deep-sea sediments of the Central Indian Basin and their growth characteristics. Fungal Divers 40: 89-102
83. Singh P, Raghukumar C, Verma P, Shouche Y (2011) Fungal community analysis in the deep-sea sediments of the Central Indian Basin by culture-independent approach. Microb Ecol 61: 507-517
84. Singh P, Raghukumar C, Meena RM, Verma P, Shouche Y (2012) Fungal diversity in deep-sea sediments revealed by culture-dependent and culture-independent approaches. Fungal Ecol 5: 543-553
85. Smit E, Leeflang P, Glandorf B, van Elsas JD, Wernars K (1999) Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis. Appl Environ Microbiol 65: 2614-2621
86. Song F, Tian X, Fan X, He X (2010) Decomposing ability of filamentous fungi on litter is involved in a subtropical mixed forest. Mycologia 102: 20-26
87. Spadaro D, Galliano A, Pellegrino C, Gilardi G, Garibaldi A, Gullino ML (2010) Dry matter, mineral composition, and commercial storage practices influence the development of skin pitting caused by Cadophora luteo-olivacea on kiwifruit 'Hayward'. J Plant Pathol 92: 349-356
88. Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157: 31-43
89. Stolk A (1955) Emericellopsis minima sp. nov. and Westerdykella ornate gen. nov., sp. nov. Trans Br Mycol Soc 38: 419-424
90. Takishita K, Tsuchiya M, Reimer JD, Maruyama T (2006) Molecular evidence demonstrating the basidiomycetous fungus Cryptococcus curvatus is the dominant microbial eukaryote in sediment at the Kuroshima Knoll methane seep. Extremophiles 10: 165-169
91. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599
92. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
93. Wafai Baaj D, Kondo N (2011) Genotyping Cephalosporium gramineum and development of a marker for molecular diagnosis. Plant Pathol 60: 730-738
94. Wang QM, Boekhout T, Bai FY (2011) Cryptococcus foliicola sp. nov. and Cryptococcus taibaiensis sp. nov., novel basidiomycetous yeast species from plant leaves. J Gen Appl Microbiol 57: 285-291
95. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Orlando, FL, p 315-322
96. Wirsel S, Leibinger W, Ernst M, Mendgen K (2001) Genetic diversity of fungi closely associated with common reed. New Phytol 149: 589-598
97. Yarwood SA, Bottomley PJ, Myrold DD (2010) Soil microbial communities associated with Douglas-fir and red alder stands at high-and low-productivity forest sites in Oregon, USA. Microb Ecol 60: 606-617
98. Yokoyama E, Arakawa M, Yamagishi K, Hara A (2006) Phylogenetic and structural analyses of the mating-type loci in Clavicipitaceae. FEMS Microbiol Lett 264: 182-191
99. Zare R, Gams W, Starink-Willemse M, Summerbell RC (2007) Gibellulopsis, a suitable genus for Verticillium nigrescens, and Musicillium, a new genus for V. theobromae. Nova Hedwigia 85: 463-489
100. Zuccaro A, Schoch CL, Spatafora JW, Kohlmeyer J, Draeger S, Mitchell JI (2008) Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl Environ Microbiol 74: 931-941