Mutualistic interactions between vitamin B 12 ‐dependent algae and heterotrophic bacteria exhibit regulation
Abstract
Many algae are auxotrophs for vitamin B(12) (cobalamin), which they need as a cofactor for B(12) -dependent methionine synthase (METH). Because only prokaryotes can synthesize the cobalamin, they must be the ultimate source of the vitamin. In the laboratory, a direct interaction between algae and heterotrophic bacteria has been shown, with bacteria supplying cobalamin in exchange for fixed carbon. Here we establish a system to study this interaction at the molecular level. In a culture of a B(12) -dependent green alga Chlamydomonas nivalis, we found a contaminating bacterium, identified by 16S rRNA analysis as Mesorhizobium sp. Using the sequenced strain of M. loti (MAFF303099), we found that it was able to support the growth of B(12) -dependent Lobomonas rostrata, another green alga, in return for fixed carbon. The two organisms form a stable equilibrium in terms of population numbers, which is maintained over many generations in semi-continuous culture, indicating a degree of regulation. However, addition of either vitamin B(12) or a carbon source for the bacteria perturbs the equilibrium, demonstrating that the symbiosis is mutualistic and facultative. Chlamydomonas reinhardtii does not require B(12) for growth because it encodes a B(12) -independent methionine synthase, METE, the gene for which is suppressed by addition of exogenous B(12) . Co-culturing C. reinhardtii with M. loti also results in reduction of METE expression, demonstrating that the bacterium can deliver the vitamin to this B(12) -independent alga. We discuss the implications of this for the widespread distribution of cobalamin auxotrophy in the algal kingdom.
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M. loti supplies vitamin B12 to L. rostrata, and in return receives fixed carbon from the microalga.
“A model interaction for the exchange of vitamin B12 is the one created between the soil rhizobiaceae Mesorhizobium loti and the freshwater green microalga Lobomonas rostrata, where M. loti supplies vitamin B12, and in return, the bacterium receives fixed carbon from the microalga [45,46,47].”
From Toward the Enhancement of Microalgal Metabolite Production through Microalgae–Bacteria Consortia (2021) · cites this paper as [45]
Cites
Lane, D. (1991) · Medical Entomology and Zoology · Cited by 7,944 · see citing works
R Factor Transfer in Rhizobium leguminosarum
Beringer, J. E. (1974) · Microbiology · doi:10.1099/00221287-84-1-188 · Cited by 2,170 · see citing works
Algae acquire vitamin B12 through a symbiotic relationship with bacteria
Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J., & Smith, A. G. (2005) · Nature · doi:10.1038/nature04056 · Cited by 1,536 · see citing works
Self-citationAlgal Physiology and Biochemistry.
Baalen, C. V., & Stewart, W. P. D. (1975) · Bulletin of the Torrey Botanical Club · doi:10.2307/2484419 · Cited by 1,494 · see citing works
The Composite Genome of the Legume Symbiont Sinorhizobium meliloti
Galibert, F., Finan, T. M., Long, S. R., Pühler, A., Abola, A. P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., Boistard, P., et al. (2001) · Science · doi:10.1126/science.1060966 · Cited by 1,181 · see citing works
(1989) · Elsevier eBooks · doi:10.1016/c2009-0-02778-0 · Cited by 1,166 · see citing works
The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use
(1990) · Choice Reviews Online · doi:10.5860/choice.27-2713 · Cited by 1,075 · see citing works
Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism
Amin, S. A., Green, D. H., Hart, M. C., Küpper, F. C., Sunda, W. G., & Carrano, C. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905512106 · Cited by 583 · see citing works
The genome of Rhizobium leguminosarum has recognizable core and accessory components
Young, J. P. W., Crossman, L. C., Johnston, A. W. B., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-4-r34 · Cited by 579 · see citing works
The biosynthesis of adenosylcobalamin (vitamin B12)
Warren, M. J., Raux, E., Schubert, H., & Escalante‐Semerena, J. C. (2002) · Natural Product Reports · doi:10.1039/b108967f · Cited by 484 · see citing works
Self-citationPathways to mutualism breakdown
Sachs, J. D., & Simms, E. L. (2006) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2006.06.018 · Cited by 436 · see citing works
Scott, J. M. (1999) · Proceedings of The Nutrition Society · doi:10.1017/s0029665199000580 · Cited by 309 · see citing works
PHYSIOLOGICAL ACCLIMATION OF MARINE PHYTOPLANKTON TO DIFFERENT NITROGEN SOURCES1
Levasseur, M. E., THOMPSON, P. A., & Harrison, P. J. H. (1993) · Journal of Phycology · doi:10.1111/j.0022-3646.1993.00587.x · Cited by 273 · see citing works
Koide, R. T., Smith, D. C., & Douglas, A. (1987) · The Bryologist · doi:10.2307/3242613 · Cited by 272 · see citing works
Wagner-Döbler, I., Ballhausen, B., Berger, M., Brinkhoff, T., Buchholz, I., Bunk, B., Cypionka, H., Daniel, R., Drepper, T., Gerdts, G., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2009.94 · Cited by 271 · see citing works
Insights into the Evolution of Vitamin B12 Auxotrophy from Sequenced Algal Genomes
Helliwell, K. E., Wheeler, G. L., Leptos, K. C., Goldstein, R. E., & Smith, A. G. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr124 · Cited by 244 · see citing works
Self-citationBetween a rock and a hard place: Trace element nutrition in Chlamydomonas
Merchant, S., Allen, M. D., Kropat, J., Moseley, J. L., Long, J. C., Tottey, S., & Terauchi, A. M. (2006) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2006.04.007 · Cited by 236 · see citing works
Vitamin B 12 and iron colimitation of phytoplankton growth in the Ross Sea
Bertrand, E. M., Saito, M. A., Rose, J. M., Riesselman, C. R., Lohan, M. C., Noble, A. E., Lee, P. A., & DiTullio, G. R. (2007) · Limnology and Oceanography · doi:10.4319/lo.2007.52.3.1079 · Cited by 229 · see citing works
Park, Y., Je, K.-W., Lee, K., Jung, S.-E., & Choi, T.-J. (2008) · Hydrobiologia · doi:10.1007/s10750-007-9152-8 · Cited by 150 · see citing works
Matsuo, Y., Suzuki, M., Kasai, H., Shizuri, Y., & Harayama, S. (2003) · Environmental Microbiology · doi:10.1046/j.1462-2920.2003.00382.x · Cited by 145 · see citing works
Purification and Properties of 5-Methyltetrahydropteroyltriglutamate-Homocysteine Transmethylase
Whitfield, C. D., Steers, E., & Weissbach, H. (1970) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)63404-0 · Cited by 138 · see citing works
Raux, E., Lanois, A., Levillayer, F., Warren, M. J., Brody, E. N., Rambach, A., & Thermes, C. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.3.753-767.1996 · Cited by 129 · see citing works
Self-citationCharacterization and Bioavailability of Vitamin B12-Compounds from Edible Algae.
Watanabe, F., Takenaka, S., Kittaka‐Katsura, H., Ebara, S., & Miyamoto, E. (2002) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.48.325 · Cited by 128 · see citing works
Regulation of phytoplankton dynamics by vitamin B12
Sañudo‐Wilhelmy, S. A., Gobler, C. J., Okbamichael, M., et al. (2006) · Geophysical Research Letters · doi:10.1029/2005gl025046 · Cited by 123 · see citing works
Gobler, C., Norman, C., Panzeca, C., Taylor, G. T., & Sañudo‐Wilhelmy, S. A. (2007) · Aquatic Microbial Ecology · doi:10.3354/ame01132 · Cited by 122 · see citing works
Llano, G. A. (1977) · Medical Entomology and Zoology · Cited by 109 · see citing works
Drummond, J. T., Huang, S., Blumenthal, R., et al. (1993) · Biochemistry · doi:10.1021/bi00087a005 · Cited by 109 · see citing works
Poole, P. S., Schofiel, N. A., Reid, C. J., et al. (1994) · Microbiology · doi:10.1099/00221287-140-10-2797 · Cited by 100 · see citing works
Eichel, J., González, J. C., Hotze, M., et al. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20655.x · Cited by 97 · see citing works
Oligotrophic bacteria enhance algal growth under iron-deficient conditions
Keshtacher-Liebso, E., Hadar, Y., & Chen, Y. (1995) · Applied and Environmental Microbiology · doi:10.1128/aem.61.6.2439-2441.1995 · Cited by 93 · see citing works
B vitamins as regulators of phytoplankton dynamics
Panzeca, C., Tovar‐Sánchez, A., Agustı́, S., Reche, I., Duarte, C. M., Taylor, G. T., & Sañudo‐Wilhelmy, S. A. (2006) · Eos · doi:10.1029/2006eo520001 · Cited by 89 · see citing works
Coenzyme B12 (cobalamin)-dependent enzymes
Neil, E., & Marsh, G. (1999) · Essays in Biochemistry · doi:10.1042/bse0340139 · Cited by 88 · see citing works
Complete Genome Structure of the Nitrogen-fixing Symbiotic Bacterium Mesorhizobium loti (Supplement)
Kaneko, T. (2000) · DNA Research · doi:10.1093/dnares/7.6.381 · Cited by 85 · see citing works
BIOCHEMICAL MUTANTS OF CHLAMYDOMONAS REINHARDI
Eversole, R. A. (1956) · American Journal of Botany · doi:10.1002/j.1537-2197.1956.tb10508.x · Cited by 78 · see citing works
Distributions of dissolved vitamin B12 and Co in coastal and open-ocean environments
Panzeca, C., Beck, A. J., Tovar‐Sánchez, A., et al. (2009) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2009.08.016 · Cited by 69 · see citing works
Scanning electron microscopy of early sporeling ontogeny of Chondrus crispus
Chen, L. C.-M., & Taylor, A. R. (1976) · Canadian Journal of Botany · doi:10.1139/b76-071 · Cited by 61 · see citing works
Cell wall carotenoids in green algae which form sporopollenins
Burczyk, J. (1986) · Phytochemistry · doi:10.1016/s0031-9422(00)81494-6 · Cited by 51 · see citing works
EFFECT OF VITAMIN CONCENTRATIONS ON GROWTH AND DEVELOPMENT OF VITAMIN‐REQUIRING ALGAE1
Carlucci, A. F., & Silbernagel, S. B. (1969) · Journal of Phycology · doi:10.1111/j.1529-8817.1969.tb02578.x · Cited by 47 · see citing works
Symbiont genomics, our new tangled bank
Medina, M., & Sachs, J. L. (2010) · Genomics · doi:10.1016/j.ygeno.2009.12.004 · Cited by 43 · see citing works
Vitamin‐B12‐Independent Methionine Synthase from a Higher Plant (Catharanthus Roseus)
Eichel, J., González, J. C., Hotze, M., et al. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.1053g.x · Cited by 36 · see citing works
Effects of cobalt and vitamin B12 on the growth of Chrysochromulina polylepis (Prymnesiophyceae)
Granéli, E., & Risinger, L. (1994) · Marine Ecology Progress Series · doi:10.3354/meps113177 · Cited by 21 · see citing works
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Ramanan, R., Kim, B.-H., Cho, D.-H., Oh, H.-M., & Kim, H.-S. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.12.003 · Cited by 1,301 · see citing works
Hena, S., Gutierrez, L., & Croué, J.-P. (2021) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.124041 · Cited by 478 · see citing works
Fuentes, J., Garbayo, I., Cuaresma, M., Montero, Z., González-del-Valle, M., & Vílchez, C. (2016) · Marine Drugs · doi:10.3390/md14050100 · Cited by 462 · see citing works
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Yao, S., Lyu, S., An, Y., Lu, J., Gjermansen, C., & Schramm, A. (2019) · Journal of Applied Microbiology · doi:10.1111/jam.14095 · Cited by 296 · see citing works
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- Authors
- Kazamia, E., Czesnick, H., Nguyen, T. T. V., Croft, M. T., Sherwood, E., Sasso, S., Hodson, S. J., Warren, M. J., & Smith, A. G.
- Affiliations
- University of Cambridge (GB)
- University of Kent (GB)
- Corresponding author
- Smith, Alison Gail
- ORCID
- Venue
- Environmental Microbiology
- Publisher
- Wiley
- Published
- 2012-03-29
- Volume
- 14
- Issue
- 6
- Pages
- 1466-1476
- ISSN
- 1462-2912 (ISSN-L)
- 1462-2920
- OpenAlex
- W2107778330
- Cited by
- 410
- References
- 41
- Citations by year
- 2026: 27 · 2025: 27 · 2024: 39 · 2023: 38 · 2022: 34 · 2021: 37 · 2020: 43 · 2019: 37 · 2018: 33 · 2017: 32 · 2016: 22 · 2015: 19 · 2014: 15 · 2013: 5 · 2012: 1
- FWCI
- 4.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Kent Academic Repository (University of Kent) (submittedVersion)
- UEA Digital Repository (University of East Anglia) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/I013164/1, BB/E024203/1)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Porphyrin Metabolism and Disorders
- Keywords
- vitamin B12, methionine synthase, Chlamydomonas nivalis, Chlamydomonas reinhardtii, Mesorhizobium loti, facultative symbiosis, population equilibrium
- MeSH terms
- Chlorophyta, Bacteria, Soil Microbiology, Symbiosis, 5-Methyltetrahydrofolate-Homocysteine S-Methyltransferase, Vitamin B 12, Heterotrophic Processes
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