Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities

FEMS Microbiology Letters

Volumn 346, Issue 2, 2013, Pages 146-154

  Lopez Velasco, Gabriela ^a   Carder, Phyllis A ^a   Welbaum, Gregory E ^a   Ponder, Monica A ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Epiphytic bacteria; Leaf microbiota; Phyllo epiphytic microbiota

Indexed keywords

RNA 16S;

ACIDOBACTERIA; ACTINOBACTERIA; ACTINOMYCETALES; ALPHAPROTEOBACTERIA; AMPLICON; ARTICLE; BACILLUS; BETAPROTEOBACTERIA; BRADYRHIZOBIACEAE; BRUCELLACEAE; CAULOBACTERACEAE; CHLAMYDIA; CHLOROFLEXI; CORYNEBACTERIUM; COTYLEDON; DEINOCOCCUS; DELTAPROTEOBACTERIA; ENTEROBACTERIACEAE; ENTEROCOCCUS; EXIGUOBACTERIUM; FIRMICUTES; GAMMAPROTEOBACTERIA; HYPHOMICROBIACEAE; METHYLOBACTERIACEAE; MICROBIAL COMMUNITY; MICROCOCCACEAE; NONHUMAN; PHYLLOSPHERE; PLANCTOMYCETES; PLANT LEAF; PLANT SEED; PLANT STRUCTURES; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMONADACEAE; PYROSEQUENCING; RHIZOBIACEAE; RHODOSPIRILLALES; SANGUIBACTER; SEEDLING; SPECIES DIVERSITY; SPECIES RICHNESS; SPERMOSPHERE; SPHINGOMONADALES; SPINACH; STAPHYLOCOCCUS; THERMUS; VERRUCOMICROBIA; XANTHOMONADALES;

ACTINOBACTERIA; BACTERIA (MICROORGANISMS); FIRMICUTES; OTUS; PROTEOBACTERIA; SPINACIA OLERACEA;

EPIPHYTIC BACTERIA; LEAF MICROBIOTA; PHYLLO EPIPHYTIC MICROBIOTA;

BACTERIA; COTYLEDON; DNA, BACTERIAL; MICROBIOTA; PLANT LEAVES; RNA, RIBOSOMAL, 16S; SEEDS; SPINACIA OLERACEA;

EID: 84882928152     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/1574-6968.12216     Document Type: Article

References (59)

1. Andrews JH & Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38: 145-180.
2. Andrews WH, Wilson CR, Poelma PL, Romero AM & Mislivec PB (1979) Bacteriological survey of sixty health foods. Appl Environ Microbiol 37: 559-566.
3. Brandl MT & Amundson R (2008) Leaf age as a risk factor in the contamination of lettuce with Escherichia coli O157:H7 and Salmonella enterica. Appl Environ Microbiol 74: 2298-2306.
4. Cankar K, Kraigher H, Ravnikar M & Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244: 341-345.
5. Carder PA (2010) Microbial communities of spinach at various stages of plant growth from seed to maturity. Thesis, Master in Science dissertation. Virginia Tech.
6. Charkowski AO, Barak JD, Sarreal CZ & Mandrell RE (2002) Differences in growth of Salmonella enterica and Escherichia coli O157:H7 on alfalfa sprouts. Appl Environ Microbiol 68: 3114-3120.
7. 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.
8. Compant S, Duffy B, Nowak J, Clément C & Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959.
9. Cottyn B, Debode J, Regalado E, Mew TW & Swings J (2009) Phenotypic and genetic diversity of rice seed-associated bacteria and their role in pathogenicity and biological control. J Appl Microbiol 107: 885-897.
10. Delmotte N, Knief C, Chaffron S et al. (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. P Natl Acad Sci USA 106: 16428-16433.
11. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG & Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8: 125.
12. Ercolani GL (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb Ecol 21: 35-48.
13. European Food Safety Authority (2011) Tracing seeds, in particular fenugreek (Trigonella foenum-graecum) seeds, in relation to the Shiga toxin-producing E. coli (STEC) O104:H4 2011 otbreaks in Germany and France. Available at: http://www.efsa.europa.eu/en/supporting/pub/176e.htm (accessed October 2012).
14. Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL & Araújo WL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287: 8-14.
15. Grice EA & Segre JA (2011) The skin microbiome. Nat Rev Microbiol 9: 244-253.
16. Guo X, van Iersel MW, Chen J, Brackett RE & Beuchat LR (2002) Evidence of association of Salmonellae with tomato plants grown hydroponically in inoculated nutrient solution. Appl Environ Microbiol 68: 3639-3643.
17. Hardoim PR, Hardoim CCP, van Overbeek LS & van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7: e30438.
18. Hernandez-Perez P & Du Toit LJ (2006) Seedborne Cladosporium variabile and Stemphylium botryosum in spinach. Plant Dis 90: 137-145.
19. Holland M, Stebbins N & Polacco JC (1992) Evidence of interactions in nitrogen metabolism between soybean and phylloplane bacteria. Plant Physiol 99: 30A.
20. Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR, Butterfield DA & Sogin ML (2007) Microbial population structures in the deep marine biosphere. Science 318: 97-100.
21. Hugenholtz P, Tyson GW, Webb RI, Wagner AM & Blackall LL (2001) Investigation of candidate division TM7, a recently recognized major lineage of the domain bacteria with no known pure-culture representatives. Appl Environ Microbiol 67: 411-419.
22. Humblot C & Guyot JP (2009) Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl Environ Microbiol 75: 4354-4361.
23. Ibekwe A & Grieve C (2004) Changes in developing plant microbial community structure as affected by contaminated water. FEMS Microbiol Lett 48: 239-248.
24. Idris R, Trifonova R, Puschenreiter M, Wenzel WW & Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70: 2667-2677.
25. Jackson EF, Echlin HL & Jackson CR (2006) Changes in the phyllosphere community of the resurrection fern, Polypodium polypodioides, associated with rainfall and wetting. FEMS Microbiol Ecol 58: 236-246.
26. Jacobs JL, Carroll TL & Sundin GW (2005) The role of pigmentation, ultraviolet radiation tolerance, and leaf colonization strategies in the epiphytic survival of phyllosphere bacteria. Microb Ecol 49: 104-113.
27. Jesus Ed da C, Susilawati E, Smith SL et al. (2010) Bacterial communities in the rhizosphere of biofuel crops grown on marginal lands as evaluated by 16S rRNA gene pyrosequences. Bioenergy Res 3: 20-27.
28. Johnston-Monje D & Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6: e20396.
29. Kadivar H & Stapleton AE (2003) Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb Ecol 45: 353-361.
30. Krimm U, Abanda-Nkpwatt D, Schwab W & Schreiber L (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol Ecol 53: 483-492.
31. Kukkurainen S, Leino A, Vähämiko S et al. (2005) Occurrence and location of endophytic bacteria in garden and wild strawberry. HortScience 40: 348-352.
32. Kulichevskaya IS, Ivanova AO, Belova SE et al. (2007) Schlesneria paludicola gen. nov., sp nov., the first acidophilic member of the order Planctomycetales, from Sphagnum-dominated boreal wetlands. Int J Syst Evol Microbiol 57: 2680-2687.
33. Lambais MR, Crowley DE, Cury JC, Bull RC & Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312: 1917.
34. Liu Z, Lozupone C, Hamady M, Bushman FD & Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35: e120.
35. Long HH, Schmidt DD & Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3: e2702.
36. López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J & Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33: 322-327.
37. Lopez-Velasco G, Welbaum GE, Boyer RR, Mane SP & Ponder MA (2011) Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16S rRNA amplicons. J Appl Microbiol 110: 1203-1214.
38. Mundt JO & Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32: 694-698.
39. Nemecek-Marshall M, MacDonald RC, Franzen JJ, Wojciechowski CL & Fall R (1995) Methanol emission from leaves (enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development). Plant Physiol 108: 1359-1368.
40. Nunes da Rocha U, Van Overbeek L & Van Elsas JD (2009) Exploration of hitherto-uncultured bacteria from the rhizosphere. FEMS Microbiol Ecol 69: 313-328.
41. Piernas V & Guirad JP (1997) Microbial hazards related to rice sprouting. Int J Food Sci Technol 32: 33-39.
42. Ragaert P, Devlieghere F & Debevere J (2007) Role of microbiological and physiological spoilage mechanisms during storage of minimally processed vegetables. Postharvest Biol Technol 44: 185-194.
43. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL & Leveau JHJ (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J 6: 1812-1822.
44. Redford AJ, Bowers RM, Knight R, Linhart Y & Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12: 2885-2893.
45. Ringelberg D, Foley K & Reynolds CM (2012) Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol 58: 67-80.
46. Roesch LF, Fulthorpe RR, Riva A et al. (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1: 283-290.
47. Ronaghi M & Elahi E (2002) Pyrosequencing for microbial typing. J Chromatogr B Analyt Technol Biomed Life Sci 782: 67-72.
48. Rosenblueth M & Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19: 827-837.
49. Ruppel S, Krumbein A & Schreiner M (2008) Composition of the phyllospheric microbial populations on vegetable plants with different glucosinolate and carotenoid compositions. Microb Ecol 56: 364-372.
50. Simon C, Wiezer A, Strittmatter AW & Daniel R (2009) Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl Environ Microbiol 75: 7519-7526.
51. Sogin ML, Morrison HG, Huber JA et al. (2006) Microbial diversity in the deep sea and the underexplored 'rare biosphere'. P Natl Acad Sci USA 103: 12115-12120.
52. Urich T, Lanzen A, Qi J, Huson DH, Schleper C & Schuster SC (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3: e2527.
53. van Overbeek L, Franke A, Nijhuis E, Groeneveld R, da Rocha U & Lotz L (2011) Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microb Ecol 62: 257-264.
54. Wang Q, Garrity GM, Tiedje JM & Cole JR (2007) Naïve Bayesian classifier for rapid assignment fo rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
55. Weiss A, Hertel C, Grothe S, Ha D & Hammes WP (2007) Characterization of the cultivable microbiota of sprouts and their potential for application as protective cultures. Syst Appl Microbiol 30: 483-493.
56. Whipps JM, Hand P, Pink D & Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105: 1744-1755.
57. Yang CH, Crowley DE, Borneman J & Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. P Natl Acad Sci USA 98: 3889-3894.
58. Yang JH, Liu HX, Zhu GM, Pan YL, Xu LP & Guo JH (2008) Diversity analysis of antagonists from rice-associated bacteria and their application in biocontrol of rice diseases. J Appl Microbiol 104: 91-104.
59. Yutthammo C, Thongthammachat N, Pinphanichakarn P & Luepromchai E (2010) Diversity and activity of PAH-degrading bacteria in the phyllosphere of ornamental plants. Microb Ecol 59: 357-368.