Skip to main content Accessibility help
Hostname: page-component-768dbb666b-9hf5z Total loading time: 1.347 Render date: 2023-02-07T06:44:48.366Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Chapter 3 - Membrane transport – nutrient uptake and protein excretion

Published online by Cambridge University Press:  04 May 2019

Byung Hong Kim
Korea Institute of Science and Technology, Seoul
Geoffrey Michael Gadd
University of Dundee
Get access
Publisher: Cambridge University Press
Print publication year: 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Primary Sources

Busch, W. & Saier, M. H. Jr. (2002). The transporter classification (TC) system, 2002. Critical Reviews in Biochemistry and Molecular Biology 37, 287337.
Eggeling, L. & Sahm, H. (2003). New ubiquitous translocators: amino acid export by Corynebacterium glutamicum and Escherichia coli. Archives of Microbiology 180, 155160.
Harold, F. M. (2005). Molecules into cells: specifying spatial architecture. Microbiology and Molecular Biology Reviews 69, 544564.
Hedfalk, K., Tornroth-Horsefield, S., Nyblom, M., Johanson, U., Kjellbom, P. & Neutze, R. (2006). Aquaporin gating. Current Opinion in Structural Biology 16, 447456.
Lolkema, J. S., Poolman, B. & Konings, W. N. (1998). Bacterial solute uptake and efflux systems. Current Opinion in Microbiology 1, 248253.
Pudlik, A. M. & Lolkema, J. S. (2011). Citrate uptake in exchange with intermediates in the citrate metabolic pathway in Lactococcus lactis IL1403. Journal of Bacteriology 193, 706714.

Secondary Sources

Krulwich, T. A., Hicks, D. B. & Ito, M. (2009). Cation/proton antiporter complements of bacteria: why so large and diverse? Molecular Microbiology 74, 257260.
Mesbah, N. M., Cook, G. M. & Wiegel, J. (2009). The halophilic alkalithermophile Natranaerobius thermophilus adapts to multiple environmental extremes using a large repertoire of Na+(K+)/H+ antiporters. Molecular Microbiology 74, 270281.
Psakis, G., Saidijam, M., Shibayama, K., Polaczek, J., Bettaney, K. E., Baldwin, J. M., Baldwin, S. A., Hope, R., Essen, L.-O., Essenberg, R. C. & Henderson, P. J. F. (2009). The sodium-dependent D-glucose transport protein of Helicobacter pylori. Molecular Microbiology 71: 391403.
Sobczak, I. & Lolkema, J. S. (2005). The 2-hydroxycarboxylate transporter family: physiology, structure, and mechanism. Microbiology and Molecular Biology Reviews 69, 665695.
Albers, S. V., Koning, S. M., Konings, W. N. & Driessen, A. J. (2004). Insights into ABC transport in archaea. Journal of Bioenergetics and Biomembranes 36, 515.
Cabezon, E. & de la Cruz, F. (2006). TrwB: an F1-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Research in Microbiology 157, 299305.
Cheng, J., Poduska, B., Morton, R. A. & Finan, T. M. (2011). An ABC-type cobalt transport system is essential for growth of Sinorhizobium melilotiat trace metal concentrations. Journal of Bacteriology 193, 44054416.
Davidson, A. L., Dassa, E., Orelle, C. & Chen, J. (2008). Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiology and Molecular Biology Reviews 72, 317364.
Erkens, G. B., Majsnerowska, M., ter Beek, J. & Slotboom, D. J. (2012). Energy coupling factor-type ABC transporters for vitamin uptake in prokaryotes. Biochemistry 51, 43904396.
Pohl, A., Devaux, P. F. & Herrmann, A. (2005). Function of prokaryotic and eukaryotic ABC proteins in lipid transport. Biochimica et Biophysica Acta 1733, 2952.
Fischer, M., Zhang, Q. Y., Hubbard, R. E. & Thomas, G. H. (2010). Caught in a TRAP: substrate-binding proteins in secondary transport. Trends in Microbiology 18, 471478.
Mulligan, C., Fischer, M. & Thomas, G. H. (2011). Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea. FEMS Microbiology Reviews 35: 6886.
Winnen, B., Hvorup, R. N. & Saier, M. H. Jr. (2003). The tripartite tricarboxylate transporter (TTT) family. Research in Microbiology 154, 457465.
Barabote, R. D. & Saier, M. H. Jr. (2005). Comparative genomic analyses of the bacterial phosphotransferase system. Microbiology and Molecular Biology Reviews 69, 608634.
Deutscher, J., Aké, F. M. D., Derkaoui, M., Zébré, A. C., Cao, T. N., Bouraoui, H., Kentache, T., Mokhtari, A., Milohanic, E. & Joyet, P. (2014). The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein–protein interactions. Microbiology and Molecular Biology Reviews 78, 231256.
Goodwin, R. A. & Gage, D. J. (2014). Biochemical characterization of a nitrogen-type phosphotransferase system reveals that enzyme EINtr integrates carbon and nitrogen signaling in Sinorhizobium meliloti. Journal of Bacteriology 196, 1901 –1907.
Pflüger-Grau, K. & Görke, B. (2010). Regulatory roles of the bacterial nitrogen-related phosphotransferase system. Trends in Microbiology 18, 205214.
Braun, V. & Braun, M. (2002). Active transport of iron and siderophore antibiotics. Current Opinion in Microbiology 5, 194201.
Llamas, M. A. & Bitter, W. (2006). Iron gate: the translocation system. Journal of Bacteriology 188, 31723174.
Schalk, I. J., Hannauer, M. & Braud, A. (2011). New roles for bacterial siderophores in metal transport and tolerance. Environmental Microbiology 13, 28442854.
Wandersman, C. & Delepelaire, P. (2004). Bacterial iron sources: from siderophores to hemophores. Annual Review of Microbiology 58, 611647.
Balhesteros, H., Shipelskiy, Y., Long, N. J., Majumdar, A., Katz, B. B., Santos, N. M., Leaden, L., Newton, S. M., Marques, M. V. & Klebba, P. E. (2017). TonB-dependent heme/hemoglobin utilization by Caulobacter crescentus HutA. Journal of Bacteriology 199, e00723–16.
Celia, H., Noinaj, N., Zakharov, S. D., Bordignon, E., Botos, I., Santamaria, M., Barnard, T. J., Cramer, W. A., Lloubes, R. & Buchanan, S. K. (2016). Structural insight into the role of the Ton complex in energy transduction. Nature 538, 6065.
Noinaj, N., Guillier, M., Barnard, T. J. & Buchanan, S. K. (2010). TonB-dependent transporters: regulation, structure, and function. Annual Review of Microbiology 64, 4360.
Postle, K. & Kadner, R. J. (2003). Touch and go: tying TonB to transport. Molecular Microbiology 49, 869882.
Du, D., van Veen, H. W. & Luisi, B. F. (2015). Assembly and operation of bacterial tripartite multidrug efflux pumps. Trends in Microbiology 23, 311319.
Hinchliffe, P., Symmons, M. F., Hughes, C. & Koronakis, V. (2013). Structure and operation of bacterial tripartite pumps. Annual Review of Microbiology 67, 221242.
Paulsen, I. T. (2003). Multidrug efflux pumps and resistance: regulation and evolution. Current Opinion in Microbiology 6, 446451.
Dalbey, R. E., Wang, P. & van Dijl, J. M. (2012). Membrane proteases in the bacterial protein secretion and quality control pathway. Microbiology and Molecular Biology Reviews 76, 311330.
Holland, I. B. (2004). Translocation of bacterial proteins – an overview. Biochimica et Biophysica Acta 1694, 516.
Pohlschroeder, M., Hartmann, E., Hand, N. J., Dilks, K. & Haddad, A. (2005). Diversity and evolution of protein translocation. Annual Review of Microbiology 59, 91111.
Pugsley, A. P., Francetic, O., Driessen, A. J. & de Lorenzo, V. (2004). Getting out: protein traffic in prokaryotes. Molecular Microbiology 52, 311.
Desvaux, M., Parham, N. J., Scott-Tucker, A. & Henderson, I. R. (2004). The general secretory pathway: a general misnomer? Trends in Microbiology 12, 306309.
Tjalsma, H., Antelmann, H., Jongbloed, J. D. H., Braun, P. G., Darmon, E., Dorenbos, R., Dubois, J. -Y. F., Westers, H., Zanen, G., Quax, W. J., Kuipers, O. P., Bron, S., Hecker, M. & van Dijl, J. M. (2004). Proteomics of protein secretion by Bacillus subtilis: separating the ‘secrets’ of the secretome. Microbiology and Molecular Biology Reviews 68, 207233.
Tsirigotaki, A., De Geyter, J., Sostaric, N., Economou, A. & Karamanou, S. (2017). Protein export through the bacterial Sec pathway. Nature Reviews Microbiology 15(1), 2136.
van der Sluis, E. O. & Driessen, A. J. M. (2006). Stepwise evolution of the Sec machinery in Proteobacteria. Trends in Microbiology 14, 105108.
Berks, B. C. (2015). The twin-arginine protein translocation pathway. Annual Review of Biochemistry 84, 843864.
Palmer, T. & Berks, B. C. (2012). The twin-arginine translocation (Tat) protein export pathway. Nature Reviews Microbiology 10, 483496.
Robinson, C. & Bolhuis, A. (2004). Tat-dependent protein targeting in prokaryotes and chloroplasts. Biochimica et Biophysica Acta 1694, 135147.
Gebhard, S. (2012). ABC transporters of antimicrobial peptides in Firmicutes bacteria – phylogeny, function and regulation. Molecular Microbiology 86, 12951317.
Buist, G., Ridder, A. N. J. A., Kok, J. & Kuipers, O. P. (2006). Different subcellular locations of secretome components of Gram-positive bacteria. Microbiology 152, 28672874.
Forster, B. M. & Marquis, H. (2012). Protein transport across the cell wall of monoderm Gram-positive bacteria. Molecular Microbiology 84, 405413.
Scheurwater, E. M. & Burrows, L. L. (2011). Maintaining network security: how macromolecular structures cross the peptidoglycan layer. FEMS Microbiology Letters 318, 19.
Blanco, L. P., Evans, M. L., Smith, D. R., Badtke, M. P. & Chapman, M. R. (2012). Diversity, biogenesis and function of microbial amyloids. Trends in Microbiology 20, 6673.
Büttner, D. (2012). Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiology and Molecular Biology Reviews 76, 262310.
Christie, P. J., Atmakuri, K., Krishnamoorthy, V., Jakubowski, S. & Cascales, E. (2005). Biogenesis, architecture, and function of bacterial type IV secretion systems. Annual Review of Microbiology 59, 451485.
Costa, T. R. D., Felisberto-Rodrigues, C., Meir, A., Prevost, M. S., Redzej, A., Trokter, M. & Waksman, G. (2015). Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nature Reviews Microbiology 13, 343359.
Dalbey, R. E. & Kuhn, A. (2012). Protein traffic in Gram-negative bacteria – how exported and secreted proteins find their way. FEMS Microbiology Reviews 36, 10231045.
Evans, L. D. B., Hughes, C. & Fraser, G. M. (2014). Building a flagellum outside the bacterial cell. Trends in Microbiology 22, 566572.
Ghosh, P. (2004). Process of protein transport by the type III secretion system. Microbiology and Molecular Biology Reviews 68, 771795.
Hachani, A., Wood, T. E. & Filloux, A. (2016). Type VI secretion and anti-host effectors. Current Opinion in Microbiology 29: 8193.
Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C. & Ala’Aldeen, D. (2004). Type V protein secretion pathway: the autotransporter story. Microbiology and Molecular Biology Reviews 68, 692744.
Kanonenberg, K., Schwarz, C. K. W. & Schmitt, L. (2013). Type I secretion systems – a story of appendices. Research in Microbiology 164, 596604.
Kim, D. S. H., Chao, Y. & Saier, M. H. Jr. (2006). Protein-translocating trimeric autotransporters of Gram-negative bacteria. Journal of Bacteriology 188, 56555667.
Lara-Tejero, M., Kato, J., Wagner, S., Liu, X. & Galán, J. E. (2011). A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331, 11881191.
Lasica, A. M., Ksiazek, M., Madej, M. & Potempa, J. (2017). The type IX secretion system (T9SS): highlights and recent insights into its structure and function. Frontiers in Cellular & Infection Microbiology 7: 215.
Stoop, E. J. M., Bitter, W. & van der Sar, A. M. (2012). Tubercle bacilli rely on a type VII army for pathogenicity. Trends in Microbiology 20, 477484.
Cuthbertson, L., Kos, V. & Whitfield, C. (2010). ABC Transporters involved in export of cell surface glycoconjugates. Microbiology and Molecular Biology Reviews 74, 341362.
Cuthbertson, L., Mainprize, I. L., Naismith, J. H. & Whitfield, C. (2009). Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiology and Molecular Biology Reviews 73, 155177.
Okuda, S., Freinkman, E. & Kahne, D. (2012). Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338, 12141217.
Putker, F., Bos, M. P. & Tommassen, J. (2015). Transport of lipopolysaccharide to the Gram-negative bacterial cell surface. FEMS Microbiology Reviews 39, 9851002.
Qiao, S., Luo, Q., Zhao, Y., Zhang, X. C. & Huang, Y. (2014). Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511, 108111.
Whitney, J. C. & Howell, P. L. (2013). Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends in Microbiology 21, 6372.
Albers, S. V., Szabo, Z. & Driessen, A. J. M. (2006). Protein secretion in the Archaea: multiple paths towards a unique cell surface. Nature Reviews Microbiology 4, 537547.
Gehring, A. M., Walker, J. E. & Santangelo, T. J. (2016). Transcription regulation in archaea. Journal of Bacteriology 198, 19061917.
Gimenez, M. I., Dilks, K. & Pohlschroder, M. (2007). Haloferax volcanii twin-arginine translocation substates include secreted soluble, C-terminally anchored and lipoproteins. Molecular Microbiology 66, 15971606.
Karr, E. A. (2014). Transcription regulation in the third domain. Advances in Applied Microbiology 89, 101133.
Kwan, D. C., Thomas, J. R. & Bolhuis, A. (2008). Bioenergetic requirements of a Tat-dependent substrate in the halophilic archaeon Haloarcula hispanica. FEBS Journal 275(24), 61596167.
Pohlschroder, M., Gimenez, M. I. & Jarrell, K. F. (2005). Protein transport in Archaea: Sec and twin arginine translocation pathways. Current Opinion in Microbiology 8, 713719.
Saleh, M., Song, C., Nasserulla, S. & Leduc, L. G. (2010). Indicators from archaeal secretomes. Microbiological Research 165, 110.
Abdul Ajees, A., Yang, J. & Rosen, B. (2011). The ArsD As(III) metallochaperone. BioMetals 24, 391399.
Bleriot, C., Effantin, G., Lagarde, F., Mandrand-Berthelot, M.-A. & Rodrigue, A. (2011). RcnB is a periplasmic protein essential for maintaining intracellular Ni and Co concentrations in Escherichia coli. Journal of Bacteriology 193, 37853793.
Braymer, J. J. & Giedroc, D. P. (2014). Recent developments in copper and zinc homeostasis in bacterial pathogens. Current Opinion in Chemical Biology 19, 5966.
Chacon, K. N., Mealman, T. D., McEvoy, M. M. & Blackburn, N. J. (2014). Tracking metal ions through a Cu/Ag efflux pump assigns the functional roles of the periplasmic proteins. Proceedings of the National Academy of Sciences of the USA 111, 1537315378.
Chandrangsu, P., Rensing, C. & Helmann, J. D. (2017). Metal homeostasis and resistance in bacteria. Nature Reviews Microbiology 15, 338350.
Furukawa, K., Ramesh, A., Zhou, Z., Weinberg, Z., Vallery, T., Winkler, W. C. & Breaker, R. R. (2015). Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Molecular Cell 57, 10881098.
Osman, D., Patterson, C. J., Bailey, K., Fisher, K., Robinson, N. J., Rigby, S. E. J. & Cavet, J. S. (2013). The copper supply pathway to a Salmonella Cu, Zn-superoxide dismutase (SodCII) involves P1B-type ATPase copper efflux and periplasmic CueP. Molecular Microbiology 87, 466477.
Cited by

Save book to Kindle

To save this book to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats