Roles of UndA and MtrC of Shewanella putrefaciens W3-18-1 in iron reduction

BMC Microbiology

Jizhong Zhou¹  Dongru Qiu³  Jingrong Chen²  Yunfeng Yang⁴ 

[1] Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA;Institute for Environmental Genomics and Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73019, USA;Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China;State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China

关键词: c-type cytochrome;    Iron reduction;    Shewanella putrefaciens W3-18-1;   

Others  :  1142605
DOI  :  10.1186/1471-2180-13-267

 received in 2013-05-28, accepted in 2013-11-20,  发布年份 2013

【 摘 要 】

Background

The completion of genome sequencing in a number of Shewanella species, which are most renowned for their metal reduction capacity, offers a basis for comparative studies. Previous work in Shewanella oneidensis MR-1 has indicated that some genes within a cluster (mtrBAC-omcA-mtrFED) were involved in iron reduction. To explore new features of iron reduction pathways, we experimentally analyzed Shewanella putrefaciens W3-18-1 since its gene cluster is considerably different from that of MR-1 in that the gene cluster encodes only four ORFs.

Results

Among the gene cluster, two genes (mtrC and undA) were shown to encode c-type cytochromes. The ΔmtrC deletion mutant revealed significant deficiencies in reducing metals of Fe₂O₃, α-FeO(OH), β-FeO(OH), ferric citrate, Mn(IV) and Co(III), but not organic compounds. In contrast, no deficiency of metal reduction was observed in the ΔundA deletion mutant. Nonetheless, undA deletion resulted in progressively slower iron reduction in the absence of mtrC and fitness loss under the iron-using condition, which was indicative of a functional role of UndA in iron reduction.

Conclusions

These results provide physiological and biochemical evidences that UndA and MtrC of Shewanella putrefaciens W3-18-1 are involved in iron reduction.

【 授权许可】

   
2013 Yang et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Shi L, Squier TC, Zachara JM, Fredrickson JK: Respiration of metal (hydr) oxides by Shewanella and Geobacter: a key role for multihaem c‒type cytochromes. Mol Microbiol 2007, 65(1):12-20.
• [2]Tiedje JM: Shewanella—the environmentally versatile genome. Nat Biotechnol 2002, 20(11):1093-1094.
• [3]Viamajala S, Peyton BM, Sani RK, Apel WA, Petersen JN: Toxic effects of chromium (VI) on anaerobic and aerobic growth of shewanella oneidensis MR‒1. Biotechnol Progr 2004, 20(1):87-95.
• [4]Lovley DR, Holmes DE, Nevin KP: Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 2004, 49:219-286.
• [5]Ziemke F, Brettar I, Höfle M: Stability and diversity of the genetic structure of a Shewanella putrefaciens population in the water column of the central Baltic. Aquat Microb Ecol 1997, 13:63-74.
• [6]Gao H, Obraztova A, Stewart N, Popa R, Fredrickson JK, Tiedje JM, Nealson KH, Zhou J: Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int J Syst Evol Microbiol 2006, 56(8):1911-1916.
• [7]Shi L, Chen B, Wang Z, Elias DA, Mayer MU, Gorby YA, Ni S, Lower BH, Kennedy DW, Wunschel DS, et al.: Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 2006, 188(13):4705-4714.
• [8]Lower BH, Yongsunthon R, Shi L, Wildling L, Gruber HJ, Wigginton NS, Reardon CL, Pinchuk GE, Droubay TC, Boily JF, et al.: Antibody recognition force microscopy shows that outer membrane cytochromes OmcA and MtrC are expressed on the exterior surface of Shewanella oneidensis MR-1. Appl Environ Microbiol 2009, 75(9):2931-2935.
• [9]Myers JM, Myers CR: Isolation and sequence of omcA, a gene encoding a decaheme outer membrane cytochrome c of Shewanella putrefaciens MR-1, and detection of omcA homologs in other strains of S. putrefaciens. Biochim Biophys Acta 1998, 1373(1):237-251.
• [10]Myers JM, Myers CR: Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 2001, 67(1):260-269.
• [11]Beliaev AS, Saffarini DA, McLaughlin JL, Hunnicutt D: MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 2001, 39(3):722-730.
• [12]Coursolle D, Gralnick JA: Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 2010, 77(4):995-1008.
• [13]Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, et al.: Towards environmental systems biology of Shewanella. Nat Rev Microbiol 2008, 6(8):592-603.
• [14]Myers C, Nealson KH: Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 1988, 240:1319-1321.
• [15]Stapleton RD, Sabree ZL, Palumbo AV, Moyer CL, Devol AH, Roh Y, Zhou JZ: Metal reduction at cold temperatures by Shewanella isolates from various marine environments. Aquat Microb Ecol 2005, 38(1):81-91.
• [16]Yang Y, Harris DP, Luo F, Xiong W, Joachimiak M, Wu L, Dehal P, Jacobsen J, Yang Z, Palumbo AV, et al.: Snapshot of iron response in Shewanella oneidensis by gene network reconstruction. BMC Genomics 2009, 10:131. BioMed Central Full Text
• [17]Yang Y, McCue LA, Parsons AB, Feng S, Zhou J: The tricarboxylic acid cycle in Shewanella oneidensis is independent of Fur and RyhB control. BMC Microbiol 2010, 10:264. BioMed Central Full Text
• [18]Yang Y, Harris DP, Luo F, Wu L, Parsons AB, Palumbo AV, Zhou J: Characterization of the Shewanella oneidensis fur gene: roles in iron and acid tolerance response. BMC Genomics 2008, 9(Suppl 1):S11. BioMed Central Full Text
• [19]Link AJ, Phillips D, Church GM: Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 1997, 179(20):6228-6237.
• [20]Saltikov CW, Newman DK: Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci USA 2003, 100(19):10983-10988.
• [21]Wan XF, Verberkmoes NC, McCue LA, Stanek D, Connelly H, Hauser LJ, Wu L, Liu X, Yan T, Leaphart A, et al.: Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J Bacteriol 2004, 186(24):8385-8400.
• [22]Anderson MJ: A new method for non‒parametric multivariate analysis of variance. Austral Ecol 2001, 26(1):32-46.
• [23]Yang Y, Wu L, Lin Q, Yuan M, Xu D, Yu H, Hu Y, Duan J, Li X, He Z: Responses of the functional structure of soil microbial community to livestock grazing in the Tibetan alpine grassland. Glob Change Biol 2013, 19(2):637-648.
• [24]Carter P: Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal Biochem 1971, 40:450-458.
• [25]Sorensen J: Reduction of ferric iron in anaerobic, marine sediment and interaction with reduction of nitrate and sulfate. Appl Environ Microbiol 1982, 43(2):319-324.
• [26]Thomas PE, Ryan D, Levin W: Improved staining procedure for detection of Peroxidase-Activity of Cytochrome-P-450 on Sodium Dodecyl-Sulfate Polyacrylamide Gels. Anal Biochem 1976, 75(1):168-176.
• [27]Konstantinidis KT, Serres MH, Romine MF, Rodrigues JLM, Auchtung J, Mccue LA, Lipton MS, Obraztsova A, Giometti CS, Nealson KH, et al.: Comparative systems biology across an evolutionary gradient within the Shewanella genus. Proc Natl Acad Sci USA 2009, 106(37):15909-15914.
• [28]Gao H, Wang X, Yang ZK, Palzkill T, Zhou J: Probing regulon of ArcA in Shewanella oneidensis MR-1 by integrated genomic analyses. BMC Genomics 2008, 9:42. BioMed Central Full Text
• [29]Zhao JS, Deng Y, Manno D, Hawari J: Shewanella spp. genomic evolution for a cold marine lifestyle and in-situ explosive biodegradation. PLoS One 2010, 5(2):e9109.
• [30]Salas EC, Berelson WM, Hammond DE, Kampf AR, Nealson KH: The impact of bacterial strain on the products of dissimilatory iron reduction. Geochim Cosmochim Ac 2010, 74(2):574-583.
• [31]Pinchuk GE, Ammons C, Culley DE, Li SMW, McLean JS, Romine MF, Nealson KH, Fredrickson JK, Beliaev AS: Utilization of DNA as a sole source of phosphorus, carbon, and energy by Shewanella spp.: ecological and physiological implications for dissimilatory metal reduction. Appl Environ Microb 2008, 74(4):1198-1208.
• [32]Edwards MJ, Hall A, Shi L, Fredrickson JK, Zachara JM, Butt JN, Richardson DJ, Clarke TA: The crystal structure of the extracellular 11-heme Cytochrome UndA reveals a conserved 10-heme motif and defined binding site for Soluble Iron Chelates. Structure 2012, 20(7):1275-1284.
• [33]Shi L, Belchik SM, Wang Z, Kennedy DW, Dohnalkova AC, Marshall MJ, Zachara JM, Fredrickson JK: Identification and characterization of UndAHRCR-6, an outer membrane endecaheme c-type cytochrome of Shewanella sp. strain HRCR-6. Appl Environ Microbiol 2011, 77(15):5521-5523.
• [34]Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K, Ray R, Wu P, Johnson BJ, Biddle EM, Marshall MJ, et al.: The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanal 2010, 22(7–8):856-864.
• [35]Clarke TA, Edwards MJ, Gates AJ, Hall A, White GF, Bradley J, Reardon CL, Shi L, Beliaev AS, Marshall MJ, et al.: Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci USA 2011, 108(23):9384-9389.