The DOI matches its Crossref record; 67 of the 67 references it cites were found in a registry or an index.
Metabolic cross-feeding via intercellular nanotubes among bacteria
Open accessAbstract
Bacteria frequently exchange metabolites by diffusion through the extracellular environment, yet it remains generally unclear whether bacteria can also use cell–cell connections to directly exchange nutrients. Here we address this question by engineering cross-feeding interactions within and between Acinetobacter baylyi and Escherichia coli, in which two distant bacterial species reciprocally exchange essential amino acids. We establish that in a well-mixed environment E. coli, but likely not A. baylyi, can connect to other bacterial cells via membrane-derived nanotubes and use these to exchange cytoplasmic constituents. Intercellular connections are induced by auxotrophy-causing mutations and cease to establish when amino acids are externally supplied. Electron and fluorescence microscopy reveal a network of nanotubular structures that connects bacterial cells and enables an intercellular transfer of cytoplasmic materials. Together, our results demonstrate that bacteria can use nanotubes to exchange nutrients among connected cells and thus help to distribute metabolic functions within microbial communities. Some bacteria can form nanotubes to transfer proteins and plasmids between neighbouring cells. Here, the authors show that nanotubes can also mediate the exchange of cytoplasmic amino acids between cells of the same or different bacterial species.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
Datsenko, K. A., & Wanner, B. L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120163297 · Cited by 14,782
Construction of Escherichia coli K‐12 in‐frame, single‐gene knockout mutants: the Keio collection
Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., & Mori, H. (2006) · Molecular Systems Biology · doi:10.1038/msb4100050 · Cited by 7,858
Escherichia Coli and Salmonella: Typhimurium Cellular and Molecular Biology
Neidhardt, F. C., & Ingraham, J. L. (1987) · Medical Entomology and Zoology · Cited by 4,089
Lenski, R. E., Rose, M. R., Simpson, S. C., & Tadler, S. C. (1991) · The American Naturalist · doi:10.1086/285289 · Cited by 1,580
Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P., Bingen, E., Bonacorsi, S., Bouchier, C., Bouvet, O., et al. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000344 · Cited by 1,181
Andersen, J. B., Sternberg, C., Poulsen, L. K., Bjørn, S. P., Givskov, M., & Molin, S. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.6.2240-2246.1998 · Cited by 1,033
Bassler, B. L., & Losick, R. (2006) · Cell · doi:10.1016/j.cell.2006.04.001 · Cited by 983
Bacterial outer membrane vesicles and the host–pathogen interaction
Kuehn, M. J., & Kesty, N. C. (2005) · Genes & Development · doi:10.1101/gad.1299905 · Cited by 951
Microbial syntrophy: interaction for the common good
Morris, B. E. L., Henneberger, R., Huber, H., & Moissl-Eichinger, C. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12019 · Cited by 920
Membrane vesicles traffic signals and facilitate group activities in a prokaryote
Mashburn, L. M., & Whiteley, M. (2005) · Nature · doi:10.1038/nature03925 · Cited by 842
A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont
Huber, H., Hohn, M. J., Rachel, R., Fuchs, T., Wimmer, V. C., & Stetter, K. O. (2002) · Nature · doi:10.1038/417063a · Cited by 825
Gene Recombination in Escherichia Coli
LEDERBERG, J., & TATUM, E. L. (1946) · Nature · doi:10.1038/158558a0 · Cited by 608
E. coli Genome Manipulation by P1 Transduction
Thomason, L. C., Costantino, N., & Court, D. L. (2007) · Current Protocols in Molecular Biology · doi:10.1002/0471142727.mb0117s79 · Cited by 592
Intercellular Nanotubes Mediate Bacterial Communication
Dubey, G. P., & Ben-Yehuda, S. (2011) · Cell · doi:10.1016/j.cell.2011.01.015 · Cited by 564
Comparison of 61 Sequenced Escherichia coli Genomes
Lukjancenko, O., Wassenaar, T. M., & Ussery, D. W. (2010) · Microbial Ecology · doi:10.1007/s00248-010-9717-3 · Cited by 532
The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism
Waters, E., Hohn, M. J., Ahel, I., Graham, D. E., Adams, M. D., Barnstead, M., Beeson, K. Y., Bibbs, L., Bolanos, R., Keller, M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1735403100 · Cited by 518
Total bacterial diversity in soil and sediment communities—A review
Torsvik, V, Sørheim, R., & Goksøyr, J. (1996) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01574690 · Cited by 517
Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology
Tseng, T.-T., Tyler, B. M., & Setubal, J. C. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-s1-s2 · Cited by 517
The global, ppGpp‐mediated stringent response to amino acid starvation in Escherichia coli
Traxler, M. F., Summers, S. M., Nguyen, H., Zacharia, V. M., Hightower, G. A., Smith, J. T., & Conway, T. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06229.x · Cited by 517
The exploitation of mutualisms
Bronstein, J. L. (2001) · Ecology Letters · doi:10.1046/j.1461-0248.2001.00218.x · Cited by 516
Defined spatial structure stabilizes a synthetic multispecies bacterial community
Kim, H. J., Boedicker, J. Q., Choi, J. W., & Ismagilov, R. F. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807935105 · Cited by 479
Rules of Engagement: Interspecies Interactions that Regulate Microbial Communities
Little, A. E. F., Robinson, C. J., Peterson, S. B., Raffa, K. F., & Handelsman, J. (2008) · Annual Review of Microbiology · doi:10.1146/annurev.micro.030608.101423 · Cited by 407
Special delivery: vesicle trafficking in prokaryotes
Mashburn‐Warren, L. M., & Whiteley, M. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05272.x · Cited by 391
Rosenzweig, R. F., Sharp, R. R., Treves, D. S., & Adams, J. (1994) · Genetics · doi:10.1093/genetics/137.4.903 · Cited by 360
Functional characterization of extracellular vesicles produced by Bacteroides gingivalis
Grenier, D., & Mayrand, D. (1987) · Infection and Immunity · doi:10.1128/iai.55.1.111-117.1987 · Cited by 357
Volkmer, B., & Heinemann, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023126 · Cited by 351
What traits are carried on mobile genetic elements, and why?
Rankin, D. J., Rocha, E. P. C., & Brown, S. P. (2011) · Heredity · doi:10.1038/hdy.2010.24 · Cited by 346
Vesicle-Mediated Transfer of Virulence Genes from Escherichia coli O157:H7 to Other Enteric Bacteria
Yaron, S., Kolling, G. L., Simon, L., & Matthews, K. R. (2000) · Applied and Environmental Microbiology · doi:10.1128/aem.66.10.4414-4420.2000 · Cited by 338
Unraveling Microbial Interactions in Food Fermentations: from Classical to Genomics Approaches
Sieuwerts, S., de Bok, F. A. M., Hugenholtz, J., & van Hylckama Vlieg, J. E. T. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00113-08 · Cited by 337
Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria
Pande, S., Merker, H., Bohl, K., Reichelt, M., Schuster, S., de Figueiredo, L. F., Kaleta, C., & Kost, C. (2014) · The ISME Journal · doi:10.1038/ismej.2013.211 · Cited by 321
Self-citationA complete collection of single‐gene deletion mutants of Acinetobacter baylyi ADP1
de Berardinis, V., Vallenet, D., Castelli, V., Besnard, M., Pinet, A., Cruaud, C., Samair, S., Lechaplais, C., Gyapay, G., Richez, C., et al. (2008) · Molecular Systems Biology · doi:10.1038/msb.2008.10 · Cited by 302
The Genotypic View of Social Interactions in Microbial Communities
Mitri, S., & Richard Foster, K. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133307 · Cited by 297
Synergistic interactions in the microbial world
Schink, B. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020579004534 · Cited by 294
Ecology and Physics of Bacterial Chemotaxis in the Ocean
Stocker, R., & Seymour, J. R. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00029-12 · Cited by 285
Kato, S., Kowashi, Y., & Demuth, D. R. (2002) · Microbial Pathogenesis · doi:10.1006/mpat.2001.0474 · Cited by 276
Bacterial Contact-Dependent Delivery Systems
Hayes, C. S., Aoki, S. K., & Low, D. A. (2010) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091449 · Cited by 257
Geomicrobiology: How Molecular-Scale Interactions Underpin Biogeochemical Systems
Newman, D. K., & Banfield, J. F. (2002) · Science · doi:10.1126/science.1010716 · Cited by 252
Kin Discrimination and Cooperation in Microbes
Strassmann, J. E., Gilbert, O. M., & Queller, D. C. (2011) · Annual Review of Microbiology · doi:10.1146/annurev.micro.112408.134109 · Cited by 233
D'Souza, G., Waschina, S., Pande, S., Bohl, K., Kaleta, C., & Kost, C. (2014) · Evolution · doi:10.1111/evo.12468 · Cited by 231
Self-citationMicrobial metabolic exchange—the chemotype-to-phenotype link
Phelan, V. V., Liu, W.-T., Pogliano, K., & Dorrestein, P. C. (2012) · Nature Chemical Biology · doi:10.1038/nchembio.739 · Cited by 223
Cellâcell signalling in bacteria: not simply a matter of quorum
Boyer, M., & Wisniewski-Dyé, F. (2009) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2009.00745.x · Cited by 210
Horizontal Gene Pool: Bacterial Plasmids and Gene Spread
Thomas, C. M. (2000) · Medical Entomology and Zoology · Cited by 193
Mechanism of intercellular molecular exchange in heterocyst‐forming cyanobacteria
Mullineaux, C. W., Mariscal, V., Nenninger, A., Khanum, H., Herrero, A., Flores, E., & Adams, D. G. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.66 · Cited by 170
Benomar, S., Ranava, D., Cárdenas, M. L., Trably, E., Rafrafi, Y., Ducret, A., Hamelin, J., Lojou, E., Steyer, J.-P., & Giudici-Orticoni, M.-T. (2015) · Nature Communications · doi:10.1038/ncomms7283 · Cited by 169
The role of bacterial outer membrane vesicles for intra‐ and interspecies delivery
Berleman, J., & Auer, M. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12048 · Cited by 168
The Mechanism of DNA Transfer in the Mating System of an Archaebacterium
Rosenshine, I., Tchelet, R., & Mevarech, M. (1989) · Science · doi:10.1126/science.2818746 · Cited by 159
Vanstockem, M., Michiels, C. W., Vanderleyden, J., & Gool, A. P. V. (1987) · Applied and Environmental Microbiology · doi:10.1128/aem.53.2.410-415.1987 · Cited by 158
Cell-to-Cell Transfer of Bacterial Outer Membrane Lipoproteins
Nudleman, E., Wall, D., & Kaiser, D. (2005) · Science · doi:10.1126/science.1112440 · Cited by 155
Dynamic Behavior of Salmonella‐Induced Membrane Tubules in Epithelial Cells
Drecktrah, D., Levine‐Wilkinson, S., Dam, T., Winfree, S., Knodler, L. A., Schroer, T. A., & Steele‐Mortimer, O. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00830.x · Cited by 145
Jander, G., Norris, S. R., Joshi, V., Fraga, M., Rugg, A., Yu, S., Li, L., & Last, R. L. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02140.x · Cited by 140
Remis, J. P., Wei, D., Gorur, A., Zemla, M., Haraga, J., Allen, S., Witkowska, H. E., Costerton, J. W., Berleman, J. E., & Auer, M. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12187 · Cited by 139
Zamenhof, S., & Eichhorn, H. H. (1967) · Nature · doi:10.1038/216456a0 · Cited by 137
Schleper, C., Holz, I., Janekovic, D., Murphy, J., & Zillig, W. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.15.4417-4426.1995 · Cited by 134
Jahn, U., Gallenberger, M., Paper, W., Junglas, B., Eisenreich, W., STETTER, K. O., Rachel, R., & Huber, H. (2007) · Journal of Bacteriology · doi:10.1128/jb.01731-07 · Cited by 125
Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
Pathak, D. T., Wei, X., Bucuvalas, A., Haft, D. H., Gerloff, D. L., & Wall, D. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002626 · Cited by 112
The Spatial Distribution of Microbes in the Environment
Franklin, R. B., & Mills, A. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6216-2 · Cited by 97
Simulating bacterial clustering around phytoplankton cells in a turbulent ocean
Bowen, J. D., Stolzenbach, K. D., & Chisholm, S. W. (1993) · Limnology and Oceanography · doi:10.4319/lo.1993.38.1.0036 · Cited by 97
Ducret, A., Fleuchot, B., Bergam, P., & Mignot, T. (2013) · eLife · doi:10.7554/elife.00868 · Cited by 82
Archaeal symbionts and parasites
Moissl‐Eichinger, C., & Huber, H. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.04.016 · Cited by 75
Evolving the Division of Labour: Generalists, Specialists and Task Allocation
Wahl, L. M. (2002) · Journal of Theoretical Biology · doi:10.1006/jtbi.2002.3133 · Cited by 60
Meyer, D. H., & Fives-Taylor, P. M. (1993) · Infection and Immunity · doi:10.1128/iai.61.11.4933-4936.1993 · Cited by 53
Evidence for particle-induced horizontal gene transfer and serial transduction between bacteria
Chiura, H. X., Kogure, K., Hagemann, S., Ellinger, A., & Velimirov, B. (2011) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2011.01077.x · Cited by 48
Close encounters: contact‐dependent interactions in bacteria
Konovalova, A., & Søgaard‐Andersen, L. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07711.x · Cited by 47
Design and Characterization of Auxotrophy-Based Amino Acid Biosensors
Bertels, F., Merker, H., & Kost, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041349 · Cited by 47
Self-citationGetting in Touch with Your Friends
Marx, C. J. (2009) · Science · doi:10.1126/science.1173088 · Cited by 40
Cited by
Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., Belzer, C., Delgado Palacio, S., Arboleya Montes, S., Mancabelli, L., et al. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-17 · Cited by 1,950
Odamaki, T., Kato, K., Sugahara, H., Hashikura, N., Takahashi, S., Xiao, J.-Z., Abe, F., & Osawa, R. (2016) · BMC Microbiology · doi:10.1186/s12866-016-0708-5 · Cited by 1,521
Happy together: microbial communities that hook up to swap electrons
Lovley, D. R. (2017) · The ISME Journal · doi:10.1038/ismej.2016.136 · Cited by 384
Glycan Utilization and Cross-Feeding Activities by Bifidobacteria
Turroni, F., Milani, C., Duranti, S., Mahony, J., van Sinderen, D., & Ventura, M. (2018) · Trends in Microbiology · doi:10.1016/j.tim.2017.10.001 · Cited by 263
Weiss, T. L., Young, E. J., & Ducat, D. C. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.10.009 · Cited by 152
Metadata
- Authors
- Pande, S., Shitut, S., Freund, L., Westermann, M., Bertels, F., Colesie, C., Bischofs, I. B., & Kost, C.
- Venue
- Nature Communications
- Published
- 2015-02-23
- Volume
- 6
- Issue
- 1
- Pages
- 6238-6238
- ISSN
- 2041-1723 (ISSN-L)
- OpenAlex
- W2018672567
- Cited by
- 273
- References
- 67
- FWCI
- 18.09
- Type
- journal article
- Language
- en
- Open access
- gold
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.