Few vitamins are as likely to cause explosive relationships as B12.
A limited fraction of all marine microorganisms—mainly species of bacteria and archaea—synthesize the vitamin. These self-sufficient prototrophs are consumed by larger organisms, which are in turn eaten by ones that are larger still. Progressively, vitamin B12 spreads itself throughout the ocean food web, ensuring that tuna and tube worms alike can grow, synthesize essential proteins, and altogether perform the functions of life.
B12, however, is a scarce commodity in many marine ecosystems. In an article published in 2012 in the Proceedings of the National Academy of Sciences, researchers sampled water from the Pacific Ocean to analyze the prevalence of B vitamins. Their findings show that hundreds of kilometers of coastline in California and Baja California have undetectably low levels of vitamin B12, reflecting a widespread limitation to producing the molecule: millions of marine bacteria are auxotrophs for B12, unable to synthesize the entire vitamin.
Now, as more recent research reveals two species of B12 auxotrophs that can cooperate to synthesize the complete molecule, scientists’ understanding of marine vitamin synthesis is changing.
In a study published in Nature, researchers from the University of Oldenburg and the University of California, San Diego, analyzed two species of bacteria from the Colwellia and Roseovarius genera, which inhabit the North Sea. Their experiment, which reveals an intricate sharing of molecules between the two species, reveals a complex—and sometimes virulent—relationship.
The sharing of B12 between organisms is a well-known phenomenon in marine biology. Prior experiments, however, focus on organisms that exchange fully-formed vitamin B12 molecules. This study, which demonstrates that bacteria can exchange smaller building blocks of B12 in order to synthesize the complete molecule collaboratively, provides new insight into marine trophisms.
To test if the Colwellia and Roseovarius species could exchange, or cross-feed, individually-synthesized components of the B12 molecule, researchers first made a growth medium absent of any components of the vitamin. Then, after harvesting and fluorescently staining the two species, the bacteria were grown in culture together, allowing for visualization of potential cross-feeding. After three days, researchers detected the presence of B12 in the culture medium, indicating that the two bacterial species, neither of which can synthesize a full B12 molecule on their own, found a way to collaboratively synthesize the vitamin. Because researchers confirmed the absence of vitamin components at the start of the experiment, the later presence of B12 could only derive from the exchange of molecules and joint synthesis of the compound between the two bacterial species.
B12, the most chemically complex of the vitamins, is structured around a central cobalt ion. Two further molecules, called ligands, attach to this central ion to give the molecule its basic structure. The corrin ligand, a ring-shaped structure made of carbon, hydrogen, and nitrogen, encircles the cobalt ion to form the bulk of the B12 molecule. Researchers designated the second attached ligand, a benzimidazole molecule, the lower ligand, as it is the minor component of B12.
Owing to the complexity of the B12 molecule, the bacteria’s joint B12 synthesis occurred in several steps. First, the Colwellia species synthesized the lower ligand, which acted as the smaller building block for vitamin B12 construction. The Roseovarius species’ synthesis of the corrin ligand, the larger building block, then prompted the Colwellia species to release the smaller building block into the growth medium. To produce a complete vitamin B12 molecule, the Roseovarius species uptook the smaller building block and facilitated its bonding with the larger.
Bacteria from the Roseovarius species now had access to a fully functional vitamin B12 molecule. The Colwellia species, on the other hand, needed to use a more unusual strategy to acquire the synthesized B12. Following the molecule’s synthesis, the Colwellia bacteria activated a bacteriophage, a virus that exclusively infects bacteria, encoded within the Roseovarius species’ genome. Phages might be thought of as the hijackers of the virus world. After taking over a bacterium’s internal machinery, they rapidly replicate thanks to their bacterial victim’s now commandeered resources. After several replication cycles, phages typically induce the lysis, or bursting, of a host bacterium and move on to infect surrounding cells.
In the case of the B12 experiment, the Roseovarius species met a similar explosive fate. This lysis of infected bacteria enabled the release of B12 into the growth medium, allowing the Colwellia species to uptake the vitamin and use it to grow and synthesize essential proteins. Researchers noted a rapid growth of the Colwellia population after the infection of the Roseovarius species, which they attributed to the Colwellia bacteria gaining access to the released vitamin B12.
The Colwellia-induced infection of the Roseovarius species provides a new insight into the complexity of marine bacterial interactions. This observed exchange of metabolic building blocks, researchers say, could be a widespread phenomenon throughout marine and terrestrial ecosystems and opens new avenues of research for the future.
References:
Bertrand, E.M., McCrow, J.P., Moustafa, A., Zheng, H., McQuaid, J.B., Delmont, T.O., Post, A.F., Sipler, R.E., Spackeen, J.L., Xu, K., Bronk, D.A., Hutchins, D.A. and Allen, A.E. (2015). ‘Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge’, Proceedings of the National Academy of Sciences of the United States of America, 112(32), 9938–9943, available: https://doi.org/10.1073/pnas.1501615112
Kasman L.M. and Porter, L.D. (2024). Bacteriophages, Treasure Island, Florida: StatPearls Publishing, available: https://www.ncbi.nlm.nih.gov/books/NBK493185/
Sañudo-Wilhelmy, S. A., Cutter, L. S., Durazo, R., Smail, E. A., Gómez-Consarnau, L., Webb, E. A., Prokopenko, M. G., Berelson, W. M. and Karl, D. M. (2012). ‘Multiple B-vitamin depletion in large areas of the coastal ocean’, Proceedings of the National Academy of Sciences of the United States of America, 109(35), 14041–14045, available: https://doi.org/10.1073/pnas.1208755109
Watanabe, F. and Bito, T. (2018). ‘Vitamin B12 sources and microbial interaction’, Experimental biology and medicine, 243(2), 148–158, available: https://doi.org/10.1177/1535370217746612
Wienhausen, G., Moraru, C., Bruns, S., Tran, D.Q., Sultana, S., Wilkes, H., Dlugosch, L., Azam, F. and Simon, M. (2024). ‘Ligand cross-feeding resolves bacterial vitamin B12 auxotrophies’, Nature, 629, 886–892, available: https://doi.org/10.1038/s41586-024-07396-y