Skip to main content
SpringerLink
Log in

Mixotrophic bacteria for environmental detoxification of contaminated waste and wastewater

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Mixotrophic bacteria provide a desirable alternative to the use of classical heterotrophic or chemolithoautotrophic bacteria in environmental technology, particularly under limiting nutrients conditions. Their bi-modal ability of adapting to inorganic or organic carbon feed and sulfur, nitrogen, or even heavy metal stress conditions are attractive features to achieve efficient bacterial activity and favorable operation conditions for the environmental detoxification or remediation of contaminated waste and wastewater. This review provides an overview on the state of the art and summarizes the metabolic traits of the most promising and emerging non-model mixotrophic bacteria for the environmental detoxification of contaminated wastewater and waste containing excess amounts of limiting nutrients. Although mixotrophic bacteria usually function with low organic carbon sources, the unusual capabilities of mixotrophic electroactive exoelectrogens and electrotrophs in bioelectrochemical systems and in microbial electrosynthesis for accelerating simultaneous metabolism of inorganic or organic C and N, S or heavy metals are reviewed. The identification of the mixotrophic properties of electroactive bacteria and their capability to drive mono- or bidirectional electron transfer processes are highly exciting and promising aspects. These aspects provide an appealing potential for unearthing new mixotrophic exoelectrogens and electrotrophs, and thus inspire the next generation of microbial electrochemical technology and mixotrophic bacterial metabolic engineering.

Key points

• Mixotrophic bacteria efficiently and simultaneously remove C and N, S or heavy metals.

• Exoelectrogens and electrotrophs accelerate metabolism of C and N, S or heavy metals.

• New mixotrophic exoelectrogens and electrotrophs should be discovered and exploited.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bacelar-Nicolau P, Johnson DB (1999) Leaching of pyrite by acidophilic heterotrophic iron-oxidizing bacteria in pure and mixed cultures. Appl Environ Microbiol 65:585–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bai Y, Su J, Wen Q, Huang T, Chang Q, Ali A (2020) Characterization and mechanism of Mn(II)-based mixotrophic denitrifying bacterium (Cupriavidus sp. HY129) in remediation of nitrate (NO3−-N) and manganese (Mn(II)) contaminated groundwater. J Hazard Mater 408:124414

    Article  PubMed  CAS  Google Scholar 

  • Belchik SM, Kennedy DW, Dohnalkova AC, Wang Y, Sevinc PC, Wu H, Lin Y, Lu HP, Fredrickson JK, Shi L (2011) Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77:4035–4041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blázquez E, Gabriel D, Baeza JA, Guisasola A (2016) Treatment of high-strength sulfate wastewater using an autotrophic biocathode in view of elemental sulfur recovery. Water Res 105:395–405

    Article  PubMed  CAS  Google Scholar 

  • Blázquez E, Gabriel D, Baeza JA, Guisasola A (2017) Evaluation of key parameters on simultaneous sulfate reduction and sulfide oxidation in an autotrophic biocathode. Water Res 123:301–310

    Article  PubMed  CAS  Google Scholar 

  • Bock E, Koops HP, Möller UC, Rudert M (1990) A new facultatively nitrite oxidizing bacterium, nitrobacter vulgaris sp. nov. Arch Microbiol 153:105–110

    Article  Google Scholar 

  • Cai Z, Huang L, Quan X, Zhao Z, Shi Y, Li Puma G (2020) Acetate production from inorganic carbon (HCO3−) in photo-assisted biocathode microbial electrosynthesis systems using WO3/MoO3/g-C3N4 heterojunctions and Serratia marcescens species. Appl Catal B-Environ 267:118611

    Article  CAS  Google Scholar 

  • Chaerun SK, Putri FY, Mubarok MZ, Minwal WP, Ichlas ZT (2017) Bioleaching of supergene porphyry copper ores from Sungai Mak Gorontalo of Indonesia by an iron- and sulfur-oxidizing mixotrophic bacterium. Solid State Phenom 262:20–23

    Article  Google Scholar 

  • Chaerun SK, Putri EA, Mubarok MZ (2020) Bioleaching of Indonesian galena concentrate with an iron- and sulfur-oxidizing mixotrophic bacterium at room temperature. Front Microbiol 11:557548

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng KY, Ginige MP, Kaksonen AH (2012) Ano-cathodophilic biofilm catalyzes both anodic carbon oxidation and cathodic denitrification. Environ Sci Technol 46:10372–10378

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Shen J, Huang L, Pan Y, Quan X (2016) Enhanced Cd(II) removal with simultaneous hydrogen production in biocathode microbial electrolysis cells in the presence of acetate or NaHCO3. Int J Hydrog Energy 41:13368–13379

    Article  CAS  Google Scholar 

  • Coma M, Puig S, Pous N, Balaguer MD, Colprim J (2013) Biocatalyzed sulphate removal in a BES cathode. Bioresour Technol 130:218–223

    Article  CAS  PubMed  Google Scholar 

  • Cui Y, Chen X, Pan Z, Wang Y, Xu Q, Bai J, Jia H, Zhou J, Yong X, Wu X (2020) Biosynthesized iron sulfide nanoparticles by mixed consortia for enhanced extracellular electron transfer in a microbial fuel cell. Bioresour Technol 318:124095

    Article  CAS  PubMed  Google Scholar 

  • Crane KW, Grover JP (2010) Coexistence of mixotrophs, autotrophs and heterotrophs in planktonic microbial communities. J Theor Biol 262:517–527

    Article  PubMed  Google Scholar 

  • Dinarieva TY, Zhuravleva AE, Pavlenko OA, Tsaplina IA, Netrusov AI (2010) Ferrous iron oxidation in moderately thermophilic acidophile Sulfobacillus sibiricus N1T. Can J Microbiol 56:803–808

    Article  CAS  PubMed  Google Scholar 

  • Dominguez-Benetton X, Varia JC, Pozo G, Modin O, Ter Heijne A, Fransaer J, Rabaey K (2018) Metal recovery by microbial electro-metallurgy. Prog Mater Sci 94:435–461

    Article  CAS  Google Scholar 

  • Goebel BM, Stackebrandt E (1994) Cultural and phylogenetic analysis of mixed microbial populations found in natural and commercial bioleaching environments. Appl Environ Microbiol 60:1614–1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Chen C, Lee DJ, Wang A, Gao D, Ren N (2014) Coupled carbon, sulfur and nitrogen cycles of mixotrophic growth of Pseudomonas sp. C27 under denitrifying sulfide removal conditions. Bioresour Technol 171:120–126

    Article  CAS  PubMed  Google Scholar 

  • Gregory KB, Lovley DR (2005) Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ Sci Technol 39:8943–8947

    Article  CAS  PubMed  Google Scholar 

  • Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6:596–604

    Article  CAS  PubMed  Google Scholar 

  • Hassan M, Wei H, Qiu H, Jaafry SWH, Su Y, Xie B (2018) Power generation and pollutants removal from landfill leachate in microbial fuel cell: variation and influence of anodic microbiomes. Bioresour Technol 247:434–442

    Article  CAS  PubMed  Google Scholar 

  • Hedrich S, Schippers A (2021) Distribution of acidophilic microorganisms in natural and man-made acidic environments. Curr Issues Mol Biol 40:25–48

    Article  PubMed  Google Scholar 

  • Hou X, Huang L (2020) Synergetic magnetic field and loaded Fe3O4 for simultaneous efficient acetate production and Cr(VI) removal in microbial electrosynthesis systems. Chem Eng J Adv 2:100019

    Article  Google Scholar 

  • Hou X, Huang L, Zhou P, Tian F, Tao Y, Li Puma G (2019) Electrosynthesis of acetate from inorganic carbon (HCO3−) with simultaneous hydrogen production and Cd(II) removal in multifunctional microbial electrosynthesis systems (MES). J Hazard Mater 371:463–473

    Article  CAS  PubMed  Google Scholar 

  • Hou J, Huang L, Zhou P, Qian Y, Li N (2020) Understanding the interdependence of strain of electrotroph, cathode potential and initial Cu(II) concentration for simultaneous Cu(II) removal and acetate production in microbial electrosynthesis systems. Chemosphere 243:125317

    Article  CAS  PubMed  Google Scholar 

  • Hou X, Huang L, Zhou P (2021) Synergetic interaction of magnetic field and loaded magnetite for enhanced acetate production in biocathode of microbial electrosynthesis system. Int J Hydrog Energy 46:7183–7194

    Article  CAS  Google Scholar 

  • Huang L, Liu Y, Yu L, Quan X, Chen G (2015) A new clean approach for production of cobalt dihydroxide from aqueous Co(II) using oxygen-reducing biocathode microbial fuel cells. J Clean Prod 86:441–446

    Article  CAS  Google Scholar 

  • Huang C, Liu Q, Chen C, Chen F, Zhao Y, Gao L, Liu W, Zhou J, Li Z, Wang A (2017) Elemental sulfur recovery and spatial distribution of functional bacteria and expressed genes under different carbon/nitrate/sulfide loadings in up-flow anaerobic sludge blanket reactors. J Hazard Mater 324:48–53

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Xue H, Zhou Q, Zhou P, Quan X (2018) Imaging and distribution of Cd(II) ions in electrotrophs and its response to current and electron transfer inhibitor in microbial electrolysis cells. Sensor Actuat B-Chem 255:244–254

    Article  CAS  Google Scholar 

  • Huang L, Tian F, Pan Y, Shan L, Shi Y, Logan BE (2019) Mutual benefits of acetate and mixed tungsten and molybdenum for their efficient removal in 40 L microbial electrolysis cells. Water Res 162:358–368

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Liu Q, Li Z, Ma X, Hou Y, Ren N, Wang A (2021a) Relationship between functional bacteria in a denitrification desulfurization system under autotrophic, heterotrophic, and mixotrophic conditions. Water Res 188:116526

  • Huang L, Song S, Cai Z, Zhou P, Li Puma G (2021b) Efficient conversion of bicarbonate (HCO3−) to acetate and simultaneous heavy metal Cr(VI) removal in photo-assisted microbial electrosynthesis systems combining WO3/MoO3/g-C3N4 heterojunctions and Serratia marcescens electrotroph. Chem Eng J 406:126786

  • Inoue T, Kamimura K, Sugio T (2000) Isolation and some properties of a mesophilic and mixotrophic iron-oxidizing bacterium, OKM-9. Biosci Biotechnol Biochem 64:2059–2067

    Article  CAS  PubMed  Google Scholar 

  • Ishiki K, Okada K, Le DQ, Shiigi H, Nagaoka T (2017) Investigation concerning the formation process of gold nanoparticles by Shewanella oneidensis MR-1. Anal Sci 33:129–131

    Article  CAS  PubMed  Google Scholar 

  • Johnson DB, Okibe N, Wakeman K, Liu Y (2008) Effect of temperature on the bioleaching of chalcopyrite concentrates containing different concentrations of silver. Hydrometallurgy 94:42–47

    Article  CAS  Google Scholar 

  • Kashima H, Regan JM (2015) Facultative nitrate reduction by electrode-respiring Geobacter metallireducens biofilms as a competitive reaction to electrode reduction in a bioelectrochemical system. Environ Sci Technol 49:3195–3202

    Article  CAS  PubMed  Google Scholar 

  • Khanongnuch R, Di Capua F, Lakaniemi AM, Rene ER, Lens PNL (2019) H2S removal and microbial community composition in an anoxic biotrickling filter under autotrophic and mixotrophic conditions. J Hazard Mater 367:397–406

    Article  CAS  PubMed  Google Scholar 

  • Khetkorn W, Baebprasert W, Lindblad P, Incharoensakdi A (2012) Redirecting the electron flow towards the nitrogenase and bidirectional Hox-hydrogenase by using specific inhibitors results in enhanced H2 production in the cyanobacterium Anabaena siamensis TISTR 8012. Bioresour Technol 118:265–271

    Article  CAS  PubMed  Google Scholar 

  • Kim YH, Park YJ, Song SH, Yoo YJ (2007) Nitrate removal without carbon source feeding by permeabilized Ochrobactrum anthropi SY509 using an electrochemical bioreactor. Enzy Microb Technol 41:663–668

    Article  CAS  Google Scholar 

  • Kim KY, Rossi R, Regan JM, Logan BE (2021) Enumeration of exoelectrogens in microbial fuel cell effluents fed acetate or wastewater substrates. Biochem Eng J 165:107816

    Article  CAS  Google Scholar 

  • Kong F, Wang A, Ren H, Huang L, Xu M, Tao H (2014) Improved dechlorination and mineralization of 4-chlorophenol in a sequential biocathode-bioanode bioelectrochemical system with mixed photosynthetic bacteria. Bioresour Technol 158:32–38

    Article  CAS  PubMed  Google Scholar 

  • Kong W, Huang L, Quan X, Zhao Z, Li Puma G (2021) Efficient production of acetate from inorganic carbon (HCO3−) in microbial electrosynthesis systems incorporating Ag3PO4/g-C3N4 anaerobic photo-assisted biocathodes. Appl Catal B-Environ 284:119696

    Article  CAS  Google Scholar 

  • Kouki S, Saidi N, M’hiri F, Nasr H, Cherif H, Ouzari H, Hassen A (2011) Isolation and characterization of facultative mixotrophic ammonia-oxidizing bacteria from constructed wetlands. J Environ Sci 23:1699–1708

    Article  CAS  Google Scholar 

  • Larkin JM (1980) Isolation of Thiothrix in pure culture and observation of a filamentous epiphyte on Thiothrix. Curr Microbiol 4:155–158

    Article  Google Scholar 

  • Lawson CE, Nuijten GHL, de Graaf RM, Jacobson TB, Pabst M, Stevenson DM, Jetten MSM, Noguera DR, McMahon KD, Amador-Noguez D, Lücker S (2021) Autotrophic and mixotrophic metabolism of an anammox bacterium revealed by in vivo 13C and 2H metabolic network mapping. ISME J 15:673–687

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Li J, Feng G, Li Z (2016) New genomic insights into “Entotheonella” symbionts in Theonella swinhoei: mixotrophy, anaerobic adaptation, resilience, and interaction. Front Microbiol 7:1333

    PubMed  PubMed Central  Google Scholar 

  • Liu Q, Huang C, Chen X, Wu Y, Lv S, Wang A (2020) Succession of functional bacteria in a denitrification desulphurisation system under mixotrophic conditions. Environ Res 188:109708

    Article  CAS  PubMed  Google Scholar 

  • Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381

    Article  CAS  PubMed  Google Scholar 

  • Logan BE, Rossi R, Ragab A, Saikaly PE (2019) Electroactive microorganisms in bioelectrochemical systems. Nat Rev Microbiol 17:307–319

    Article  CAS  PubMed  Google Scholar 

  • Lontoh S, Dispirito AA, Krema CL, Whittaker MR, Hooper AB, Semrau JD (2000) Differential inhibition in vivo of ammonia monooxygenase, soluble methane monooxygenase and membrane-associated methane monooxygenase by phenylacetylene. Environ Microbiol 2:485–494

    Article  CAS  PubMed  Google Scholar 

  • Lovejoy C, Legendre L, Therriault JC, Tremblay JÉ, Klein B, Ingram RG (2000) Growth and distribution of marine bacteria in relation to nanoplankton community structure. Deep-Sea Res II 47:461–487

    Article  CAS  Google Scholar 

  • Luedin SM, Storelli N, Danza F, Roman S, Wittwer M, Pothier JF, Tonolla M (2019) Mixotrophic growth under micro-oxic conditions in the purple sulfur bacterium “Thiodictyon syntrophicum”. Front Microbiol 10:384

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo H, Fu S, Liu G, Zhang R, Bai Y, Luo X (2014) Autotrophic biocathode for high efficient sulfate reduction in microbial electrolysis cells. Bioresour Technol 167:462–468

    Article  CAS  PubMed  Google Scholar 

  • Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Sinninghe Damsté JS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107:13479–13484

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahmood Q, Zheng P, Cai J, Wu D, Hu B, Li J (2007) Anoxic sulfide biooxidation using nitrite as electron acceptor. J Hazard Mater 147:249–256

    Article  CAS  PubMed  Google Scholar 

  • Marshall KT, Morris RM (2013) Isolation of an aerobic sulfur oxidizer from the SUP05/Arctic96BD-19 clade. ISME J 7:452–455

    Article  CAS  PubMed  Google Scholar 

  • Marshall MJ, Beliaev AS, Dohnalkova AC, Kennedy DW, Shi L, Wang Z, Boyanov MI, Lai B, Kemner KM, McLean JS, Reed SB, Culley DE, Bailey VL, Simonson CJ, Saffarini DA, Romine MF, Zachara JM, Fredrickson JK (2006) c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. Plos Biol 4:e268

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mason J, Kelly DP (1988) Mixotrophic and autotrophic growth of Thiobacillus acidophilus on tetrathionate. Arch Microbiol 149:317–323

    Article  CAS  Google Scholar 

  • McGlannan MF, Makemson JC (1990) HCO3− fixation by naturally occurring tufts and pure cultures of Thiothrix nivea. Appl Environ Microbiol 56:730–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller TL, Wolin M (1974) A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 27:985–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miran W, Jang J, Nawaz M, Shahzad A, Jeong SE, Jeon CO, Lee DS (2017) Mixed sulfate-reducing bacteria-enriched microbial fuel cells for the treatment of wastewater containing copper. Chemosphere 189:134–142

    Article  CAS  PubMed  Google Scholar 

  • Mladenovska Z, Ahring BK (1997) Mixotrophic growth of two thermophilic Methanosarcina strains, Methanosarcina thermophila TM-1 and Methanosarcina sp. SO-2P, on methanol and hydrogen/carbon dioxide. Appl Microbiol Biotechnol 48:385–388

    Article  CAS  Google Scholar 

  • Mubarok MZ, Winarko R, Chaerun SK, Rizki IN, Ichlas ZT (2017) Improving gold recovery from refractory gold ores through biooxidation using iron-sulfur-oxidizing/sulfur-oxidizing mixotrophic bacteria. Hydrometallurgy 168:69–75

    Article  CAS  Google Scholar 

  • Narayan KD, Sabat SC, Das SK (2017) Mechanism of electron transport during thiosulfate oxidation in an obligately mixotrophic bacterium Thiomonas bhubaneswarensis strain S10 (DSM 18181T). Appl Microbiol Biotechnol 101:1239–1252

    Article  CAS  PubMed  Google Scholar 

  • Oh SE, Yoo YB, Young JC, Kim IS (2001) Effect of organics on sulfur-utilizing autotrophic denitrification under mixotrophic conditions. J Biotechnol 92:1–8

    Article  CAS  PubMed  Google Scholar 

  • Padden AN, Kelly DP, Wood AP (1998) Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis. Arch Microbiol 169:249–256

    Article  CAS  PubMed  Google Scholar 

  • Palovaara J, Akram N, Baltar F, Bunse C, Forsberg J, Pedrós-Alió C, González JM, Pinhassi J (2014) Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria. Proc Natl Acad Sci USA 111:E3650–E3658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng C, Sundman A, Bryce C, Catrouillet C, Borch T, Kappler A (2018) Oxidation of Fe(II)-organic matter complexes in the presence of the mixotrophic nitrate-reducing Fe(II)-oxidizing bacterium Acidovorax sp. BoFeN1. Environ Sci Technol 52:5753–5763

    Article  CAS  PubMed  Google Scholar 

  • Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin S, Yu L, Yang Z, Li M, Clough T, Wrage-Mönnig N, Hu C, Liu B, Chen S, Zhou S (2019) Electrodes donate electrons for nitrate reduction in a soil matrix via DNRA and denitrification. Environ Sci Technol 53:2002–2012

    Article  CAS  PubMed  Google Scholar 

  • Rabaey K, Boon N, Siciliano SD, Verhaege M, Verstraete W (2004) Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 70:5373–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rabaey K, van de Sompel K, Maignien L, Boon N, Aelterman P, Clauwaert P, De Schamphelaire L, Pham HT, Vermeulen J, Verhaege M, Lens P, Verstraete W (2006) Microbial fuel cells for sulfide removal. Environ Sci Technol 40:5218–5224

    Article  CAS  PubMed  Google Scholar 

  • Robertson LA, Kuenen JG (1984) Aerobic denitrification: a controversy revived. Arch Microbiol 139:351–354

    Article  CAS  Google Scholar 

  • Sahinkaya E, Kilic A, Calimlioglu B, Toker Y (2013) Simultaneous bioreduction of nitrate and chromate using sulfur-based mixotrophic denitrification process. J Hazard Mater 262:234–239

    Article  CAS  PubMed  Google Scholar 

  • Sanders RW, Gast RJ (2012) Bacterivory by phototrophic picoplankton and nanoplankton in Arctic waters. FEMS Microbiol Ecol 82:242–253

    Article  CAS  PubMed  Google Scholar 

  • Sanwani E, Mirahati RZ, Chaerun SK (2017) Recovery of copper from pyritic copper ores using a biosurfactant-producing mixotrophic bacterium as bioflotation reagent. Solid State Phenom 262:181–184

    Article  Google Scholar 

  • Shah V, Chang BX, Morris RM (2017) Cultivation of a chemoautotroph from the SUP05 clade of marine bacteria that produces nitrite and consumes ammonium. ISME J 11:263–271

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Huang L, Zhou P, Quan X, Li Puma G (2017) Correlation between circuital current, Cu(II) reduction and cellular electron transfer in EAB isolated from Cu(II)-reduced biocathodes of microbial fuel cells. Bioelectrochemistry 114:1–7

    Article  CAS  PubMed  Google Scholar 

  • Song X, Huang L, Lu H, Zhou P, Wang M, Li N (2020) An external magnetic field for efficient acetate production from inorganic carbon in Serratia marcescens catalyzed cathode of microbial electrosynthesis system. Biochem Eng J 155:107467

    Article  CAS  Google Scholar 

  • Spring S, Riedel T, Spröer C, Yan S, Harder J, Fuchs BM (2013) Taxonomy and evolution of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria: description of Luminiphilus syltensis gen. nov., sp. nov., reclassification of Haliea rubra as Pseudohaliea rubra gen. nov., comb. nov., and emendation of Chromatocurvus halotolerans. BMC Microbiol 13:118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srinivasan VN, Butler CS (2017) Ecological and transcriptional responses of anode-respiring communities to nitrate in a microbial fuel cell. Environ Sci Technol 51:5334–5342

    Article  CAS  PubMed  Google Scholar 

  • Strittmatter AW, Liesegang H, Rabus R, Decker I, Amann J, Andres S (2009) Genome sequence of Desulfobacterium autotrophicum HRM2, a marine sulfate reducer oxidizing organic carbon completely to carbon dioxide. Environ Microbiol 11:1038–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su W, Zhang L, Tao Y, Zhan G, Li D, Li D (2012) Sulfate reduction with electrons directly driven from electrodes in bioelectrochemical systems. Electrochem Commun 22:37–40

    Article  CAS  Google Scholar 

  • Su J, Ma M, Huang T, Ma F, Shao S, Lu J, Deng L (2017) Characteristics of autotrophic and heterotrophic denitrification by the strain Pseudomonas sp. H117. Geomicrobiol J 34:45–52

    Article  CAS  Google Scholar 

  • Su J, Gao C, Huang T, Gao Y, Bai X, He L (2019) Characterization and mechanism of the Cd(II) removal by anaerobic denitrification bacterium Pseudomonas sp. H117. Chemosphere 222:970–979

    Article  CAS  Google Scholar 

  • Sun Z, Pang B, Xi J, Hu H (2019) Screening and characterization of mixotrophic sulfide oxidizing bacteria for odorous surface water bioremediation. Bioresour Technol 290:121721

    Article  CAS  PubMed  Google Scholar 

  • Sun S, Huang L, Song X, Zhou P (2021) An external magnetic field moderating Cr(VI) stress for simultaneous enhanced acetate production and Cr(VI) removal in microbial electrosynthesis system. Environ Res 193:110550

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Xue H, Huang L, Zhou P, Yang W, Quan X, Yuan J (2017) Fluorescent probe based subcellular distribution of Cu(II) ions in living electrotrophs isolated from Cu(II)-reduced biocathodes of microbial fuel cells. Bioresour Technol 225:316–325

    Article  CAS  PubMed  Google Scholar 

  • Tavormina PL, Orphan VJ, Kalyuzhnaya MG, Jetten MSM, Klotz MG (2011) A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs. Environ Microbiol Rep 3:91–100

    Article  CAS  PubMed  Google Scholar 

  • Teng W, Liu G, Luo H, Zhang R, Xiang Y (2016) Simultaneous sulfate and zinc removal from acid wastewater using an acidophilic and autotrophic biocathode. J Hazard Mater 304:159–165

    Article  CAS  PubMed  Google Scholar 

  • Tian LJ, Li WW, Zhu TT, Chen JJ, Wang WK, An PF, Zhang L, Dong JC, Guan Y, Liu DF, Zhou NQ, Liu G, Tian YC, Yu HQ (2017) Directed biofabrication of nanoparticles through regulating extracellular electron transfer. J Am Chem Soc 139:12149–12152

    Article  CAS  PubMed  Google Scholar 

  • Tong S, Zhang B, Feng C, Zhao Y, Chen N, Hao C, Pu J, Zhao L (2013) Characteristics of heterotrophic/biofilm-electrode autotrophic denitrification for nitrate removal from groundwater. Bioresour Technol 48:121–127

    Article  CAS  Google Scholar 

  • Vidal R (2017) Alcohol dehydrogenase AdhA plays a role in ethanol tolerance in model cyanobacterium Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 101:3473–3482

    Article  CAS  PubMed  Google Scholar 

  • Vilajeliu-Pons A, Koch C, Balaguer MD, Colprim J, Harnisch F, Puig S (2018) Microbial electricity driven anoxic ammonium removal. Water Res 130:168–175

    Article  CAS  PubMed  Google Scholar 

  • Wagner-Döbler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Ann Rev Microbiol 60:255–280

    Article  CAS  Google Scholar 

  • Wang Q, Huang L, Pan Y, Zhou P, Quan X, Logan BE, Chen HB (2016a) Cooperative cathode electrode and in situ deposited copper for subsequent enhanced Cd(II) removal and hydrogen evolution in bioelectrochemical systems. Bioresour Technol 200:565–571

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Xiong X, Sa N, Roje S, Chen S (2016b) Metabolic engineering of enhanced glycerol-3-phosphate synthesis to increase lipid production in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 100:6091–6101

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Huang L, Quan X, Li Puma G (2019) Sequential anaerobic and electro-Fenton processes mediated by W and Mo oxides for degradation/mineralization of azo dye methyl orange in photo assisted microbial fuel cells. Appl Catal B-Environ 245:672–680

    Article  CAS  Google Scholar 

  • Wang W, Li Z, Zeng L, Dong C, Shao Z (2020) The oxidation of hydrocarbons by diverse heterotrophic and mixotrophic bacteria that inhabit deep-sea hydrothermal ecosystems. ISME J 14:1994–2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu D, Ekama GA, Chui HK, Wang B, Cui YX, Hao TW, van Loosdrecht MC, Chen GH (2016) Large-scale demonstration of the sulfate reduction autotrophic denitrification nitrification integrated (SANI®) process in saline sewage treatment. Water Res 100:496–507

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Ren X, Owens G, Brunetti G, Zhou J, Yong X, Wei P, Jia H (2018a) A facultative electroactive chromium(VI)-reducing bacterium aerobically isolated from a biocathode microbial fuel cell. Front Microbiol 9:2883

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Zhao X, Jin M, Li Y, Li S, Kong F, Nan J, Wang A (2018b) Copper removal and microbial community analysis in single-chamber microbial fuel cell. Bioresour Technol 253:372–377

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Wang L, Jin M, Zhang K (2020) Simultaneous copper removal and electricity production and microbial community in microbial fuel cells with different cathode catalysts. Bioresour Technol 305:123166

    Article  CAS  PubMed  Google Scholar 

  • Xafenias N, Zhang Y, Banks CJ (2013) Enhanced performance of hexavalent chromium reducing cathodes in the presence of Shewanella oneidensis MR-1 and lactate. Environ Sci Technol 47:4512–4520

    Article  CAS  PubMed  Google Scholar 

  • Xing W, Li J, Li D, Hu J, Deng S, Cui Y, Yao H (2018) Stable-isotope probing reveals the activity and function of autotrophic and heterotrophic denitrifiers in nitrate removal from organic-limited wastewater. Environ Sci Technol 52:7867–7875

    Article  CAS  PubMed  Google Scholar 

  • Xing D, Cheng S, Logan BE, Regan JM (2010) Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl Microbiol Biotechnol 85:1575–1587

    Article  CAS  PubMed  Google Scholar 

  • Xue H, Zhou P, Huang L, Quan X, Yuan J (2017) Cathodic Cr(VI) reduction by electrochemically active bacteria sensed by fluorescent probe. Sensor Actuat B-Chem 243:303–310

    Article  CAS  Google Scholar 

  • Xu X, Chen C, Guo H, Wang A, Ren N, Lee DJ (2016) Characterization of a newly isolated strain Pseudomonas sp. C27 for sulfide oxidation: reaction kinetics and stoichiometry. Sci Rep 6:21032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J, Zhong K, Wang S, Chen Z, Hu H, Jian Z, Wen H, Zhang H (2018) Carbon metabolism and sulfate respiration by a non-conventional Citrobacter freundii strain SR10 with potential application in removal of metals and metalloids. Inter Biodeter Biodegr 133:238–246

    Article  CAS  Google Scholar 

  • Yang C, Hua Q, Shimizu K (2002) Integration of the information from gene expression and metabolic fluxes for the analysis of the regulatory mechanisms in Synechocystis. Appl Microbiol Biotechnol 58:813–822

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa K, Kojima Y, Nakajima T, Furusawa C, Hirasawa T, Shimizu H (2011) Reconstruction and verification of a genome-scale metabolic model for Synechocystis sp. PCC6803. Appl Microbiol Biotechnol 92:347–358

    Article  CAS  PubMed  Google Scholar 

  • Yi Y, Zhao T, Xie B, Zang Y, Liu H (2020) Dual detection of biochemical oxygen demand and nitrate in water based on bidirectional Shewanella loihica electron transfer. Bioresour Technol 309:123402

    Article  CAS  PubMed  Google Scholar 

  • Zhai S, Ji M, Zhao Y, Pavlostathis SG (2021) Biotransformation of 4-hydroxybenzoic acid under nitrate-reducing conditions in a MEC bioanode. Environ Sci Technol 55:2067–2075

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Zhang Y, Su W, Jiang Y, Su M, Gao P, Li D (2014) Effects of cathode potentials and nitrate concentrations on dissimilatory nitrate reductions by Pseudomonas alcaliphila in bioelectrochemical systems. J Environ Sci 26:885–891

    Article  CAS  Google Scholar 

  • Zhao F, Rahunen N, Varcoe JR, Chandra A, Avignone-Rossa C, Thumser AE, Slade RCT (2008) Activated carbon cloth as anode for sulfate removal in a microbial fuel cell. Environ Sci Technol 42:4971–4976

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Feng C, Wang Q, Yang Y, Zhang Z, Sugiura N (2011) Nitrate removal from groundwater by cooperating heterotrophic with autotrophic denitrification in a biofilm-electrode reactor. J Hazard Mater 192:1033–1039

    Article  CAS  PubMed  Google Scholar 

  • Zhao F, Heidrich ES, Curtis TP, Dolfing J (2020) Understanding the complexity of wastewater: the combined impacts of carbohydrates and sulphate on the performance of bioelectrochemical systems. Water Res 176:115737

    Article  CAS  PubMed  Google Scholar 

  • Zuo Y, Xing D, Regan JM, Logan BE (2008) Isolation of the exoelectrogenic bacterium Ochrobactrum anthropi YZ-1 by using a U-tube microbial fuel cell. Appl Environ Microbiol 74:3130–3137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge financial support from the National Natural Science Foundation of China (Nos. 52070032 and 21777017), the Fundamental Research Funds for the Central Universities (No. DUT21LAB101), and the Programme of Introducing Talents of Discipline to Universities (B13012).

Author information

Authors and Affiliations

  1. Key Laboratory of Industrial Ecology and Environmental Engineering, Ministry of Education (MOE), School of Environmental Science and Technology, Dalian University of Technology, Dalian, 116024, China

    Liping Huang & Xin Xing

  2. College of Chemistry, Dalian University of Technology, Dalian, 116024, China

    Peng Zhou

  3. Environmental Nanocatalysis & Photoreaction Engineering, Department of Chemical Engineering, Loughborough University, Loughborough, LE11 3TU, UK

    Gianluca Li Puma

Authors
  1. Liping Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gianluca Li Puma
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.H. conceived, conceptualized, and prepared the writing—original draft. X.X. analyzed data. P.Z. validated data. G.L.P. visualized figures and wrote—reviewed and edited the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Liping Huang or Gianluca Li Puma.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, L., Xing, X., Zhou, P. et al. Mixotrophic bacteria for environmental detoxification of contaminated waste and wastewater. Appl Microbiol Biotechnol 105, 6627–6648 (2021). https://doi.org/10.1007/s00253-021-11514-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-021-11514-5

Keywords

Search

Navigation