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Protein Expression Profile of Gluconacetobacter Diazotrophicus PAL5, a Sugarcane Endophytic Plant Growth-Promoting Bacterium

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Protein Expression Profile of Gluconacetobacter Diazotrophicus PAL5, a Sugarcane Endophytic Plant Growth-Promoting Bacterium Proteomics 2008, 8, 1631–1644 DOI 10.1002/pmic.200700912 1631 RESEARCH ARTICLE Protein expression profile of Gluconacetobacter diazotrophicus PAL5, a sugarcane endophytic plant growth-promoting bacterium Leticia M. S. Lery1, 2, Ana Coelho1, 3, Wanda M. A. von Kruger1, 2, Mayla S. M. Gonc¸alves1, 3, Marise F. Santos1, 4, Richard H. Valente1, 5, Eidy O. Santos1, 3, Surza L. G. Rocha1, 5, Jonas Perales1, 5, Gilberto B. Domont1, 4, Katia R. S. Teixeira1, 6 and Paulo M. Bisch1, 2 1 Rio de Janeiro Proteomics Network, Rio de Janeiro, Brazil 2 Unidade Multidisciplinar de Genômica, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 3 Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 4 Laboratório de Química de Proteínas, Departamento de Bioquímica, Instituto de Química, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 5 Laboratório de Toxinologia, Departamento de Fisiologia e Farmacodinâmica- Instituto Oswaldo Cruz- Fundac¸ão Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brazil 6 Laboratório de Genética e Bioquímica, Embrapa Agrobiologia, Seropédica, Brazil This is the first broad proteomic description of Gluconacetobacter diazotrophicus, an endophytic Received: September 25, 2007 bacterium, responsible for the major fraction of the atmospheric nitrogen fixed in sugarcane in Revised: December 18, 2007 tropical regions. Proteomic coverage of G. diazotrophicus PAL5 was obtained by two independent Accepted: December 19, 2007 approaches: 2-DE followed by MALDI-TOF or TOF-TOF MS and 1-DE followed by chromatog- raphy in a C18 column online coupled to an ESI-Q-TOF or ESI-IT mass spectrometer. The 583 identified proteins were sorted into functional categories and used to describe potential meta- bolic pathways for nucleotides, amino acids, carbohydrates, lipids, cofactors and energy produc- tion, according to the Enzyme Commission of Enzyme Nomenclature (EC) and Kyoto Encyclo- pedia of genes and genomes (KEGG) databases. The identification of such proteins and their possible insertion in conserved biochemical routes will allow comparisons between G. diazo- trophicus and other bacterial species. Furthermore, the 88 proteins classified as conserved unknown or unknown constitute a potential target for functional genomic studies, aiming at the understanding of protein function and regulation of gene expression. The knowledge of meta- bolic fundamentals and coordination of these actions are crucial for the rational, safe and sus- tainable interference on crops. The entire dataset, including peptide sequence information, is available as Supporting Information and is the major contribution of this work. Keywords: Bacterial metabolism / Gluconacetobacter diazotrophicus / Sugarcane / Sustainable agriculture Correspondence: Leticia Miranda Santos Lery, Instituto de Biofí- Abbreviations: ADH, alcohol dehydrogenase; ALDH, aldehyde sica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, dehydrogenase; BNF, biological nitrogen fixation; EC, enzyme Av. Brigadeiro Tropowski, Centro de Ciencias da Saúde - Bloco G commission number; NAD, nicotinamide adenine dinucleotide; Lab.G1-043/Ilha do Fundão, Rio de Janeiro, Rio de Janeiro, PPP, pentose phosphate pathway; PQQ, pyrroloquinoline qui- 21949-900 Brazil none; TCA, citric acid cycle E-mail: [email protected], [email protected] Fax: 155-21-22808193 © 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.proteomics-journal.com 1632 L. M. S. Lery et al. Proteomics 2008, 8, 1631–1644 1 Introduction Other G. diazotrophicus contributions to a profitable as- sociation with the host-plants include the synthesis of the One of the growth-limiting factors for any organism is plant growth-promoting substances auxins and gibberellins nitrogen. Although the most abundant compound in at- [18–20] and of a bacteriocin, whose lysozyme-like activity in- mosphere, approximately 79%, this large reservoir of free hibits growth of the sugarcane pathogen, Xanthomonas albi- nitrogen is not available for many organisms, including lineans [21]. Moreover, G. diazotrophicus exhibits antagonistic plants [1]. Furthermore, crop production in tropical soils, activity against the phytotoxin produced by the fungus Colle- often assumed to be highly weathered and thus nutrient- trotrichum falcatum, the causal agent of red-rot, the most depleted, is mainly based on the increasing use of chemi- dreaded disease in sugarcane [22]. cal fertilizers. Since nitrogen is the main yield-limiting G. diazotrophicus also secretes a constitutively expressed factor, as much as 30% of the total fertilizers used are levansucrase (LsdA), which allows the bacterium to use nitrogenous chemicals [2]. Apart from costs, fertilizers sucrose, its natural carbon source substrate [23, 24]. Sucrose affect the balance of the global nitrogen cycle, pollute utilization by G. diazotrophicus leads to the accumulation of groundwater, and increase the risk of chemical spills and gluconic acids, which causes acidification of the media [25]. the amount of atmospheric nitrous oxide, a potent This highlights a secondary biofertilizer activity of G. diazo- “greenhouse” gas [3]. Consequently, decreasing depend- trophicus, since acidification can promote solubilization of ence on chemicals input for agricultural production is a zinc and inorganic phosphate compounds in the soil [26]. G. need. diazotrophicus is an endophyte, but has also been found in Among the environmental-friendly technologies avail- the rhizosphere [16], therefore, its solubilization activities able, great emphasis has been given to the biological nitro- might work outside and inside the host, turning the ele- gen fixation (BNF) process. The enzymatic reduction of N2 to ments in the environment promptly available to increase ammonia, unique to Bacteria and Archaea [4, 5], makes crop productivity. nitrogen available to living organisms, either directly, by as- G. diazotrophicus properties studied so far suggest it is a sociation with N2-fixing microorganisms (diazotrophs), or diazotrophic organism quite distinct from other root-asso- – indirectly, by conversion of organic nitrogen into NO3 and ciated bacteria [27]. Therefore, efforts have been made to 1 NH4 , thus making nitrogen in the soil ready for plant better understand its physiology, aiming the future develop- uptake [6]. ment of biotechnological approaches for a more sustainable Besides Rhizobium species, which establish a nitrogen- and environmentally safe crop production [28]. BNF asso- fixing symbiosis in root nodules of legume plants, there is ciated to sugarcane crops is a matter of special interest. In also a major subset of soil free-living bacteria, the endophytic Brazil, ethanol fuel produced from sugarcane is cheaper diazotrophs, which fix nitrogen when in association with than oil, just as convenient and environmentally superior plant root surfaces or within host tissues [7, 8]. Living as because it does not increase CO2 levels. Improvement in endophytes, the bacteria face less competition for nutrients, agricultural sustainability will require further exploitation of interact more intimately with the plant and are protected BNF to turn it into the major source of nitrogen for plants. from changes in the environment [9, 10]. Its advantages include renewability and independence of Microbiological survey on cultures of Brazilian sugar- fossil-based energy, whose costs and supply are affected by cane tissues showed greater diversity of diazotrophic bacteria international politics and whose manufacture, distribution than in varieties grown in countries where substantial nitro- and use require a complex infrastructure [3]. gen input is applied to the soil [11, 12]. Thus, the low-cost The characteristics of G. diazotrophicus described above high-yield production of sugarcane in Brazil is a reflection of emphasize its abilities to directly promote growth and pro- the vast extensions of cropland, the tropical sunny weather tect the sugarcane plant. However, the large-scale application plus the nitrogen-fixing activities of these endophytes. This is of selected strains of G. diazotrophicus for ethanol produc- an example of the optimization of BNF applied to crop pro- tion, with regard to a positive energy balance of the Brazilian duction, without the adverse environmental effects of fertili- biofuel program, has been hampered by inconsistent perfor- zers [11–13]. mance in field trials [29–31]. Among possible culprits is the Among the endophytic diazotrophic bacteria isolated poor knowledge regarding the molecular basis of G. diazo- from sugarcane plants, Gluconacetobacter diazotrophicus (syn. trophicus-sugarcane interaction and on the relative contribu- Acetobacter diazotrophicus) was the first described [14]. It was tion of each symbiotic partner to the biology of the intact as- isolated in 1988 from sugarcane juice-rich medium [15] and sociation. later characterized as an acid-tolerant N2-fixing, aerobic, Over the last years, the Riogene Genome Consortium Gram-negative bacterium. It has been found in roots, stems joined efforts to sequence G. diazotrophicus strain PAL5 and leaves of sugarcane plants, as well as in Cameroon grass, genomic DNA. Data analysis revealed about 3990 putative sweet potato, coffee, tea, banana, ragi, rice and pineapple ORF (Ferreira, P. C. G. et al., Riogene is a consortium set up [16]. G. diazotrophicus worldwide distribution is responsible to sequence complete genome of G. diazotrophicus
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