Abstract
A novel pigmented bacterium, initially identified as 11E, was isolated from a site historically known to have various iron-related ores. Phylogenetic analysis of this bacterial strain showed that it belongs to Serratia marcescens. This pigmented S. marcescens 11E cultured individually with glucose, acetate, and glycerol as electron donors along with the soluble electron acceptor iron (Fe) (III) citrate offered a large reduction extent (45.3 %, 31.4 %, and 13.5 %, respectively). On the other hand, when iron oxide (Fe2O3) is used as electron acceptor, the pigmented strain produced a null reduction extent. Surprisingly, the absence of prodigiosin on the bacterial surface (non-pigmented strain) resulted in a large reduction extent of the non-soluble iron form (20–49%). All these extents were comparable and, in some cases, superior to those presented in the literature. Additionally, in the present study, it was found that anthraquinone sulfonate (AQS) stimulated Fe(III) reduction of soluble and non-soluble Fe species only with pigmented S. marcescens. In contrast, in the culture media with the non-pigmented strain, the presence of AQS did not stimulate the Fe(III) reduction. These results suggest that the pigmented phenotype of S. marcescens 11E may perform non-soluble Fe(III) reduction by electron shuttling. In contrast, for the non-pigmented phenotype of this bacterium, non-soluble Fe(III) reduction seems to proceed by direct contact. Our study demonstrates that this bacterium may be used in bioreduction process of heavy metals or as a biocatalyst in bioelectrochemical devices.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams LK, Boothman C, Lloyd JR (2007) Identification and characterization of a novel acidotolerant Fe(III)-reducing bacterium from a 3000-year-old acidic rock drainage site. FEMS Microbiol Lett 268:151–157. https://doi.org/10.1111/j.1574-6968.2007.00635.x
Allard T, Menguy N, Salomon J et al (2004) Revealing forms of iron in river-borne material from major tropical rivers of the Amazon Basin (Brazil). Geochim Cosmochim Acta. https://doi.org/10.1016/j.gca.2004.01.014
APHA (1998) Water Environment Federation and American Water Works Association, In Standard methods for the examination of water and wastewater, 20th edn. Ed. Washington DC
Bonneville S, Behrends T, Van Cappellen P (2009) Solubility and dissimilatory reduction kinetics of iron(III) oxyhydroxides: a linear free energy relationship. Geochim Cosmochim Acta. https://doi.org/10.1016/j.gca.2009.06.006
Carbonell GV, Della Colleta HHM, Yano T et al (2000) Clinical relevance and virulence factors of pigmented Serratia marcescens. FEMS Immunol Med Microbiol 28:143–149. https://doi.org/10.1016/S0928-8244(00)00146-2
Chong GW, Karbelkar AA, El-Naggar MY (2018) Nature’s conductors: what can microbial multi-heme cytochromes teach us about electron transport and biological energy conversion? Curr Opin Chem Biol 47:7–17. https://doi.org/10.1016/j.cbpa.2018.06.007
Chun AY, Yunxiao L, Ashok S et al (2014) Elucidation of toxicity of organic acids inhibiting growth of Escherichia coli W. Biotechnol Bioprocess Eng 19:858–865. https://doi.org/10.1007/s12257-014-0420-y
Danevcic T, Vezjak MB, Tabor M et al (2016) Prodigiosin induces autolysins in actively grown Bacillus subtilis cells. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00027
De Araújo HWC, Fukushima K, Takaki GMC (2010) Prodigiosin production by Serratia marcescens UCP 1549 using renewable-resources as a low cost substrate. Molecules. https://doi.org/10.3390/molecules15106931
Degelmann DM, Kolb S, Dumont M et al (2009) Enterobacteriaceae facilitate the anaerobic degradation of glucose by a forest soil. FEMS Microbiol Ecol 68:312–319. https://doi.org/10.1111/j.1574-6941.2009.00681.x
Domagala A, Jarosz T, Lapkowski M (2015) Living on pyrrolic foundations - advances in natural and artificial bioactive pyrrole derivatives. Eur J Med Chem. https://doi.org/10.1016/j.ejmech.2015.06.009
Elkenawy NM, Yassin AS, Elhifnawy HN, Amin MA (2017) Optimization of prodigiosin production by Serratia marcescens using crude glycerol and enhancing production using gamma radiation. Biotechnol Rep 14:47–53. https://doi.org/10.1016/j.btre.2017.04.001
El-Naggar MY, Wanger G, Leung KM et al (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci 107:18127–18131. https://doi.org/10.1073/pnas.1004880107
Fu L, Li SW, Ding ZW et al (2016) Iron reduction in the DAMO/Shewanella oneidensis MR-1 coculture system and the fate of Fe(II). Water Res 88:808–815. https://doi.org/10.1016/j.watres.2015.11.011
Fuller SJ, McMillan DGG, Renz MB et al (2014) Extracellular electron transport-mediated Fe(iii) reduction by a community of alkaliphilic bacteria that use flavins as electron shuttles. Appl Environ Microbiol. https://doi.org/10.1128/AEM.02282-13
Gescher JS, Cordova CD, Spormann AM (2008) Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol Microbiol 68:706–719. https://doi.org/10.1111/j.1365-2958.2008.06183.x
Giri A V, Anandkumar N, Muthukumaran G, Pennathur G (2004) A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol 4:
Glombitza C, Jaussi M, Røy H et al (2015) Formate, acetate, and propionate as substrates for sulfate reduction in sub-arctic sediments of Southwest Greenland. Front Microbiol 6:1–14. https://doi.org/10.3389/fmicb.2015.00846
Grujcic D, Hesselhøj Hansen T, Husted S, et al (2018) Effect of nitrogen and zinc fertilization on zinc and iron bioavailability and chemical speciation in maize silage. doi: https://doi.org/10.1016/j.jtemb.2018.02.012
Gupta P, Diwan B (2017) Bacterial Exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnol Rep 13:58–71. https://doi.org/10.1016/j.btre.2016.12.006
Harrison A (1984) The acidophilic and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38:265–292
Hori T, Aoyagi T, Itoh H et al (2015) Isolation of microorganisms involved in reduction of crystalline iron(III) oxides in natural environments. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00386
Huang S, Jaffé P (2018) Isolation and characterization of an ammonium-oxidizing iron reducer: Acidimicrobiaceae sp. A6. PLoS One 13:. doi: https://doi.org/10.1371/journal.pone.0194007
Huang L, Feng C, Jiang H et al (2018) Reduction of structural Fe(III) in nontronite by thermophilic microbial consortia enriched from hot springs in Tengchong, Yunnan Province, China. Chem Geol 479:47–57. https://doi.org/10.1016/j.chemgeo.2017.12.028
Johnson DB, Falaga C (2014) Acidibacter ferrireducens gen. nov., sp. nov.: an acidophilic ferric iron-reducing gammaproteobacterium. doi: https://doi.org/10.1007/s00792-014-0684-3
Kulandaisamy Venil C, Lakshmanaperumalsamy P (2009) An insightful overview on microbial pigment, prodigiosin. Electron J Biotechnol 5:49–61
Kulkarni HV, Mladenov N, McKnight DM et al (2018) Dissolved fulvic acids from a high arsenic aquifer shuttle electrons to enhance microbial iron reduction. Sci Total Environ 615:1390–1395. https://doi.org/10.1016/j.scitotenv.2017.09.164
Lee JS, Kim YS, Park S et al (2011) Exceptional production of both prodigiosin and cycloprodigiosin as major metabolic constituents by a novel marine bacterium, Zooshikella rubidus S1-1. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01986-10
Lentini CJ, Wankel SD, Hansel CM (2012) Enriched iron(III)-reducing bacterial communities are shaped by carbon substrate and iron oxide mineralogy. Front Microbiol. https://doi.org/10.3389/fmicb.2012.00404
Liu L, Lee DJ, Wang A et al (2016) Isolation of Fe(III)-reducing bacterium, Citrobacter sp. LAR-1, for startup of microbial fuel cell. Int J Hydrog Energy. https://doi.org/10.1016/j.ijhydene.2015.07.072
Liu G, Qiu S, Liu B et al (2017) Microbial reduction of Fe(III)-bearing clay minerals in the presence of humic acids. Sci Rep 7:1–9. https://doi.org/10.1038/srep45354
Liu G, Yu H, Wang N et al (2018) Microbial reduction of ferrihydrite in the presence of reduced Graphene oxide materials: alteration of Fe(III) reduction rate, biomineralization product and settling behavior. Chem Geol 476:272–279. https://doi.org/10.1016/j.chemgeo.2017.11.023
Manderville RA (2001) Synthesis, proton-affinity and anti-cancer properties of the prodigiosin- group natural products. Synthesis-Stuttgart 195–218
Mullerried FKG (1944) Geología del estado de Nuevo León, 1st edn. UANL, Monterrey, N.L. 1:39–83
NOM-110-SSA1 (1994) Norma oficial mexicana. Bienes y servicios. Preparación y dilución de muestras de alimentos para su análisis microbiológico. http://www.economia-noms.gob.mx/%0Anoms/inicio.do. Accessed 20 Jan 2019
Pan W, Kan J, Inamdar S et al (2016) Dissimilatory microbial iron reduction release DOC (dissolved organic carbon) from carbon-ferrihydrite association. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2016.08.026
Parker CW, Auler AS, Barton MD et al (2018) Fe(III) Reducing microorganisms from iron ore caves demonstrate fermentative Fe(III) reduction and promote cave formation. Geomicrobiol J 35:311–322. https://doi.org/10.1080/01490451.2017.1368741
Romero-Rodríguez A, Ruiz-Villafán B, Tierrafría VH et al (2016) Carbon catabolite regulation of secondary metabolite formation and morphological differentiation in Streptomyces coelicolor. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-016-2158-9
Ruiz B, Chávez A, Forero A et al (2010) Production of microbial secondary metabolites: regulation by the carbon source. Crit Rev Microbiol 36:146–167. https://doi.org/10.3109/10408410903489576
Sarma B, Acharya C, Joshi SR (2016) Characterization of metal tolerant Serratia spp. isolates from sediments of uranium ore deposit of Domiasiat in Northeast India. Proc Natl Acad Sci India Sect B - Biol Sci 86:253–260. https://doi.org/10.1007/s40011-013-0236-0
Shi L, Dong H, Reguera G et al (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14:651–662. https://doi.org/10.1038/nrmicro.2016.93
Stern N, Mejia J, He S et al (2018) Dual role of humic substances as electron donor and shuttle for dissimilatory iron reduction. Environ Sci Technol 52:5691–5699. https://doi.org/10.1021/acs.est.7b06574
Stookey LL (1970) Ferrozine- a new spectrophotometric reagent for iron. Anal Chem 42:779–781. https://doi.org/10.1021/ac60289a016
Stubbendieck RM, Straight PD (2016) Multifaceted interfaces of bacterial competition. J Bacteriol 198:2145–2155. https://doi.org/10.1128/jb.00275-16
Thorpe CL, Morris K, Boothman C, Lloyd JR (2012) Alkaline Fe(III) reduction by a novel alkali-tolerant Serratia sp. isolated from surface sediments close to Sellafield nuclear facility, UK. FEMS Microbiol Lett. https://doi.org/10.1111/j.1574-6968.2011.02455.x
Tomat E (2016) Coordination chemistry of linear tripyrroles: promises and perils. Comment Inorg Chem. https://doi.org/10.1080/02603594.2016.1180291
Van der Zee FP, Cervantes FJ (2009) Impact and application of electron shuttles on the redox (bio)transformation of contaminants: a review. Biotechnol Adv
Venkata Mohan S, Mohanakrishna G, Reddy BP et al (2008) Bioelectricity generation from chemical wastewater treatment in mediatorless (anode) microbial fuel cell (MFC) using selectively enriched hydrogen producing mixed culture under acidophilic microenvironment. Biochem Eng J 39:121–130. https://doi.org/10.1016/j.bej.2007.08.023
Wang K, sheng YP, long DQ et al (2013) Diversity of culturable root-associated/endophytic bacteria and their chitinolytic and aflatoxin inhibition activity of peanut plant in China. World J Microbiol Biotechnol 29:1–10. https://doi.org/10.1007/s11274-012-1135-x
Wang XN, Sun GX, Li XM et al (2018) Electron shuttle-mediated microbial Fe(III) reduction under alkaline conditions. J Soils Sediments 18:159–168. https://doi.org/10.1007/s11368-017-1736-y
Zavarzina DG, Gavrilov SN, Zhilina TN (2018) Direct Fe(III) reduction from synthetic ferrihydrite by haloalkaliphilic lithotrophic sulfidogens. Microbiology 87:164–172. https://doi.org/10.1134/S0026261718020170
Zheng S, Wang B, Li Y et al (2017) Electrochemically active iron (III)-reducing bacteria in coastal riverine sediments. J Basic Microbiol 57:1045–1054. https://doi.org/10.1002/jobm.201700322
Ziegler S, Waidner B, Itoh T, et al (2013) Metallibacterium scheffleri gen. nov., sp. nov., an alkalinizing gammaproteobacterium isolated from an acidic biofilm. 1499–1504. doi: https://doi.org/10.1099/ijs.0.042986-0
Acknowledgments
The authors would like to gratefully acknowledge Facultad de Ciencias Químicas at Universidad Autónoma de Nuevo León and FEMSA Biotechnology Center at Tecnológico de Monterrey for their support with the laboratory facilities. Carlos Castillo-Zacarías acknowledges CONACYT (México) for the support provided in the form of PhD studies’ fellowship no. 309171.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
All the graphics provided in the present manuscript were made up using the program Origin 2017, produced by OriginLab Corporation, Northampton, Massachusetts.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 445 kb)
Rights and permissions
About this article
Cite this article
Castillo-Zacarías, C., Cantú-Cárdenas, M.E., López-Chuken, U.J. et al. Dissimilatory reduction of Fe(III) by a novel Serratia marcescens strain with special insight into the influence of prodigiosin. Int Microbiol 23, 201–214 (2020). https://doi.org/10.1007/s10123-019-00088-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-019-00088-y