Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants

FEMS Microbiology Ecology

Volumn 88, Issue 2, 2014, Pages 424-435

  Marques, Joana M ^a   da Silva, Thais F ^a   Vollu, Renata E ^a   Blank, Arie F ^b   Ding, Guo Chun ^c,d   Seldin, Lucy ^a   Smalla, Kornelia ^c  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^c INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^d CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bacterial communities; Denaturing gradient gel electrophoresis; Ipomoea batatas L.; Pyrosequencing; Sweet potato; Tuber rhizosphere

Indexed keywords

RNA 16S;

ARTICLE; BACTERIUM; CLASSIFICATION; DENATURING GRADIENT GEL ELECTROPHORESIS; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IPOMOEA BATATAS L.; ISOLATION AND PURIFICATION; MICROBIAL COMMUNITY; MICROBIOLOGY; PYROSEQUENCING; RHIZOSPHERE; SWEET POTATO; TUBER RHIZOSPHERE;

BACTERIAL COMMUNITIES; DENATURING GRADIENT GEL ELECTROPHORESIS; IPOMOEA BATATAS L.; PYROSEQUENCING; SWEET POTATO; TUBER RHIZOSPHERE;

BACTERIA; DENATURING GRADIENT GEL ELECTROPHORESIS; GENOTYPE; IPOMOEA BATATAS; RHIZOSPHERE; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY;

EID: 84899970731     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12313     Document Type: Article

References (57)

1. Albuquerque LC, Inoue-Nagata AK, Pinheiro B, Resende RO, Moriones E & Navas-Castillo J (2012) Genetic diversity and recombination analysis of sweepoviruses from Brazil. Virol J 9: 241.
2. Andreote FD, Araújo WL, Azevedo JL, van Elsas JD, Rocha UN & van Overbeek L (2009) Endophytic colonization of potato (Solanum tuberosum L.) by a novel competent bacterial endophyte, Pseudomonas putida strain P9, and the effect on associated bacterial communities. Appl Environ Microbiol 75: 3396-3406.
3. Araújo FF, Henning AA & Hungria M (2005) Phytohormones and antibiotics produced by Bacillus subtilis and their effects on seed pathogenic fungi and on soybean root development. World J Microbiol Biotechnol 21: 1639-1645.
4. Bais HP, Weir TL, Perry LG, Gilroy S & Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
5. Beneduzi A, Peres D, da Costa PB, Bodanese Zanettini MH & Passaglia LM (2008) Genetic and phenotypic diversity of plant-growth-promoting bacilli isolated from wheat fields in southern Brazil. Res Microbiol 159: 244-250.
6. Berendsen RL, Pieterse CMJ & Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
7. Berg G & Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68: 1-13.
8. Binh CTT, Heuer H, Gomes NCM, Kaupenjohann M & Smalla K (2010) Similar bacterial community structure and high abundance of sulfonamide resistance genes in field-scale manures. Manure: Management, Uses and Environmental Impacts (Dellaguardia CS, ed.), pp. 141-166. New Science Publishers, Hauppauge, NY.
9. Buée 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: 189-212.
10. Chen XH, Koumoutsi A, Scholz R et al. (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25: 1007-1014.
11. Costa R, Gomes NCM, Krögerrecklenfort E, Opelt K, Berg G & Smalla K (2007) Pseudomonas community structure and antagonistic potential in the rhizosphere: in-sights gained by combining phylogenetic and functional gene-based analyses. Environ Microbiol 9: 2260-2273.
12. Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK, Hamady M, Knight R & Gordon JI (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. P Natl Acad Sci USA 106: 11276-11281.
13. Dias ACF, Andreote FD, Hannula SE, Andreote FD, Silva MCP, Salles JF, Boer W, van Veen J & van Elsas JD (2013) Different selective effects on rhizosphere bacteria exerted by genetically modified versus conventional potato lines. PLoS One 8: e67948.
14. Ding GC, Heuer H & Smalla K (2012) Dynamics of bacterial communities in two unpolluted soils after spiking with phenanthrene: soil type specific and common responders. Front Microbiol 3: 290.
15. Ding GC, Pronk GJ, Babin D, Heuer H, Heister K, Kögel-Knabner I & Smalla K (2013) Mineral composition and charcoal determine the bacterial community structure in artificial soils. FEMS Microbiol Ecol 86: 15-25.
16. Duvernay WH, Chinna MS & Yencho GC (2013) Hydrolysis and fermentation of sweet potatoes for production of fermentable sugars and ethanol. Ind Crop Prod 42: 527-537.
17. Ferrari MD, Guigou M & Lareo C (2013) Energy consumption evaluation of fuel bioethanol production from sweet potato. Bioresour Technol 136: 377-384.
18. Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonça-Hagler L & Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232: 167-180.
19. Gomes NCM, Kosheleva IA, Abraham WR & Smalla K (2005) Effects of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on the soil bacterial community. FEMS Microbiol Ecol 54: 21-33.
20. Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T & Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2: 1221-1230.
21. Herschkovitz Y, Lerner A, Davidov Y, Rothballer M, Hartmann A, Okon Y & Jurkevitch E (2005) Inoculation with the plant growth promoting rhizobacterium Azospirillum brasilense causes little disturbance in the rhizosphere and rhizoplane of maize (Zea mays). Microb Ecol 50: 277-288.
22. Heuer H, Krsek M, Baker P, Smalla K & Wellington EMH (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233-3241.
23. Heuer H, Wieland J, Schönfeld J, Schönwälder A, Gomes NCM & Smalla K (2001) Bacterial community profiling using DGGE or TGGE analysis. Environmental Molecular Microbiology: Protocols and Applications (Rouchelle PA, ed.), pp. 177-190. Horizon Scientific Press, Wymondham, UK.
24. Heuer H, Kroppenstedt RM, Lottmann J, Berg G & Smalla K (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl Environ Microbiol 68: 1325-1335.
25. Hothorn T, Bretz F & Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50: 346-363.
26. Inceoglu Ö, Salles JF, van Overbeek L & van Elsas JD (2010) Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl Environ Microbiol 76: 3675-3684.
27. Inceoglu Ö, Al-Soud WA, Salles JF, Semenov AV & van Elsas JD (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 6: e23321.
28. Inceoglu Ö, Salles JF & van Elsas JD (2012) Soil and cultivar type shape the bacterial community in the potato rhizosphere. Microb Ecol 63: 460-470.
29. Khan Z & Doty SL (2009) Characterization of bacterial endophytes of sweet potato plants. Plant Soil 322: 197-207.
30. Köberl M, Müller H, Ramadan EM & Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 6: e24452.
31. Köberl M, Ramadan EM, Adam M, Cardinale M, Hallmann J, Heuer H, Smalla K & Berg G (2013) Bacillus and Streptomyces were selected as broad-spectrum antagonists against soilborne pathogens from arid areas in Egypt. FEMS Microbiol Lett 342: 168-178.
32. Kropf S, Heuer H, Grüning M & Smalla K (2004) Significance test for comparing microbial community fingerprints using pairwise similarity measures. J Microbiol Methods 57: 187-195.
33. Lee WS, Chen IC, Chang CH & Yang SS (2012a) Bioethanol production from sweet potato by co-immobilization of saccharolytic molds and Saccharomyces cerevisiae. Renewable Energy 39: 216-222.
34. Lee B, Lee S & Ryu CM (2012b) Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann Bot 110: 281-290.
35. Lerner A, Herschkovitz Y, Baudoin E, Nazaret S, Moënne-Loccoz Y, Okon Y & Jurkevitch E (2006) Effect of Azospirillum brasilense on rhizobacterial communities analyzed by denaturing gradient gel electrophoresis and automated intergenic spacer analysis. Soil Biol Biochem 38: 1212-1218.
36. Milling A, Smalla K, Xaver F, Maidl K, Schloter M & Munch JC (2004) Effects of transgenic potatoes with an altered starch composition on the diversity of soil and rhizosphere bacteria and fungi. Plant Soil 266: 23-39.
37. Oliveira Neto MA (2012) Comportamento de germoplasma de batata-doce em Sergipe. Dissertação de Mestrado. Universidade Federal do Sergipe, SE, Brazil.
38. Önneby K, Håkansson S, Pizzul L & Stenström J (2014) Reduced leaching of the herbicide MCPA after bioaugmentation with a formulated and stored Sphingobium sp. Biodegradation 25: 291-300.
39. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J & Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
40. Puspasari F, Radjasa OK, Noer AS, Nurachman Syah ZYM, van der Maarel M, Dijkhuizen L, Janecek S & Natalia D (2012) Raw starch-degrading α-amylase from Bacillus aquimaris MKSC 6.2: isolation and expression of the gene, bioinformatics and biochemical characterization of the recombinant enzyme. J Appl Microbiol 114: 108-120.
41. Rudrappa T, Czymmek KJ, Paré PW & Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148: 1547-1556.
42. Ruiz Y, Medina L, Borusiak M, Ramos N, Pinto G & Valbuena O (2013) Biodegradation of polyethoxylated nonylphenols. ISRN Microbiol. 2013: 284950.
43. 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.
44. Silveira MA (1993) Resistencia de clones de batata-doce (Ipomoea batatas L.) quanto aos nematóides do gênero Melodoigyne e aos insetos do solo. Dissertação de Mestrado em Fitotecnia. Universidade Federal de Lavras (UFLA), MG, Brazil.
45. Silveira MA (2008) Batata-doce: uma nova alternativa para a produção de etanol. Álcool combustível (Instituto Euvaldo Lodi), pp. 109-122. IEL, Brasília, Brazil.
46. Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H & Berg G (2001) Bulk and rhizosphere bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67: 4742-4751.
47. Somers E, Vanderleyden J & Srinivisam M (2004) Rhizosphere bacterial signaling: a love parade beneath our feet. Crit Rev Microbiol 30: 205-240.
48. Srichuwong S, Fujiwara M, Wang X, Seyama T, Shiroma R, Arakane M, Mukojima N & Tokuyasu K (2009) Simultaneous saccharification and fermentation (SSF) of very high gravity (VHG) potato mash for the production of ethanol. Biomass Bioenergy 33: 890-898.
49. Takai K & Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66: 5066-5072.
50. Tien CJ, Lin MC, Chiu WH & Chen CS (2013) Biodegradation of carbamate pesticides by natural rivers biofilms in different seasons and their effects on biofilm community structure. Environ Pollut 179: 95-104.
51. Tiwari R, Kalra A, Darokar MP, Chandra M, Aggarwal N & Khanuja SPS (2010) Endophytic bacteria from Ocimum sanctum and their yield enhancing capabilities. Curr Microbiol 60: 167-171.
52. van Overbeek L & van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64: 283-296.
53. Wang Q, Garrity GM, Tiedje JM & Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
54. Wang M, Shi Y, Xia X, Li D & Chen Q (2013) Life-cycle energy efficiency and environmental impacts of bioethanol production from sweet potato. Bioresour Technol 133: 285-292.
55. Weinert N, Meincke R, Gottwald C, Heuer H, Schloter M, Berg G & Smalla K (2009) Rhizosphere microbial communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differed less than those of different potato cultivars. Appl Environ Microbiol 75: 3859-3865.
56. Weinert N, Meincke R, Gottwald C, Radl V, Dong X, Schloter M, Berg G & Smalla K (2010) Effects of genetically modified potatoes with increased zeaxanthin content on the abundance and diversity of rhizobacteria with in vitro antagonistic activity do not exceed natural variability among cultivars. Plant Soil 326: 437-452.
57. Ziska LH, Runion GB, Tomecek M, Prior SA, Torbet HA & Sicher R (2009) An evaluation of cassava, sweet potato and field corn as potential carbohydrate sources for bioethanol production in Alabama and Maryland. Biomass Bioenergy 33: 1503-1508.