Microbiology

Algae and the vitamin mosaic

The requirements for vitamin B12 vary among algal species in a seemingly inexplicable pattern. A study that exploits genomic data now provides enlightenment — and evidence of symbioses with bacteria.

Animals require vitamin B12 in their diets but plants don't. Algal requirements, on the other hand, present a complicated picture. Many algae must take up vitamin B12 (like animals) whereas many others do not (like plants)1, and there is no evolutionary pattern to these requirements. Even different isolates of the same species can have different demands2.

On page 90 of this issue3, Croft et al. provide an explanation for this baffling mosaic of algal vitamin-B12 requirements. And they go a step further. For algae that require an external source of vitamin B12, they provide convincing evidence of an algal–bacterial symbiosis in which algal carbon-rich exudates are exchanged for the vitamin produced by the bacteria. For these algae, vitamin B12, they find, is an essential co-factor for an enzyme on a pathway that produces the amino acid methionine.

When algal species were first cultured more than 100 years ago, they were grown on a defined plant culture medium that lacked vitamins4. But some algae could not be grown in this way, and soil extract was added to the medium for these ‘unculturable’ organisms5. The soil provided, among other nutrients, an unrecognized source of vitamins, making it possible to culture most species of algae. In 1948, liver extract was shown to improve the growth of Euglena6 and evidence for a vitamin-B12 requirement in algae came one year later7. Shortly thereafter, Euglena and Poterioo-chromonas became important bioassay organisms for detecting vitamin-B12 deficiencies in human blood and urine samples1. By 1980, vitamin-B12 requirements were known for approximately 400 algal strains8, but after this, studies on the topic almost ceased.

Croft et al.3 have picked up the baton. They started by re-examining the vitamin-B12 requirements of some algal strains. Their results were identical to previous reports. Puzzled by the lack of an evolutionary pattern for vitamin-B12 requirements among algae, they searched for genes encoding vitamin-B12-dependent enzymes in the genomes of the green alga Chlamydomonas, the red alga Cyanidioschizon and the brown diatom Thalassiosira.

They found that Chlamydomonas and Cyanidioschizon have both a vitamin-B12-dependent methionine synthase gene (metH) and a vitamin-B12-independent methionine synthase gene (metE). Both organisms can grow without an external vitamin source. Croft et al. further showed that Chlamydomonas preferentially used the metH gene when vitamin B12 was available, but used the metE gene when vitamin B12 was absent. Conversely, they found only the vitamin-B12-dependent methionine synthase gene (metH) in the Thalassiosira genome, an alga with an absolute requirement for this vitamin9.

Presumably, the ancestors of algae had both genes, and numerous independent losses of either the metE or metH gene subsequently occurred over evolutionary time. Remarkably, descendants seem to have continued to arise almost exclusively from ancestors with both genes — which explains why we do not find lineages (as we do with plants and animals) with either one gene type or the other. The scattered losses produced the evolutionary mosaic at the level of species or even strain.

Croft et al.3 also provide evidence that a bacterium, Halomonas, upregulates the biosynthesis of vitamin B12 when in the presence of algal exudates. Many algae are members of a loose taxonomic grouping known as the protists. These are often unicellular and include such organisms as Amoeba and Paramecium. The phenomenon of endosymbiosis, in which one organism (such as a bacterium) takes up residence inside another, to mutual benefit, has been thoroughly studied in protists, especially with regard to the origins of the chloroplast and mitochondrion. But possible ectosymbioses — literally, more superficial relationships — involving bacteria and algae have received less attention.

An earlier investigation did indeed show that Thalassiosira and other marine diatoms, all of which require vitamin B12, could be grown without the vitamin when bacterial cultures were added to the diatom cultures10. Such studies hinted at the existence of a symbiotic relationship. But unlike Croft et al., the authors of this study did not identify the bacteria involved or the specific genes (or enzymes) concerned, and they did not demonstrate upregulation of a bacterial gene in response to a chemical signal from the algae.

Croft and colleagues' approach3 could profitably be adopted more broadly, because protists have a much wider variety of basic biochemical pathways than do either animals or plants. We can hope that the enzymatic pathways leading to other amino acids, sugars, lipids and so forth — which have long been known to be diverse in protists and to show similar evolutionary mosaic patterns11 — will likewise be examined using the genome data now available. It is likely that additional symbiotic vitamin-B12-producing bacteria will be identified, and that other vitamins are produced by symbiotic bacteria.

But non-symbiotic bacterial sources of vitamins may be equally or more important. For example, concentrations of vitamin B12 in the oceans vary with season, and there is strong circumstantial evidence that this vitamin is produced on the ocean floor at depths where darkness makes it unlikely that an algal–bacterial symbiosis can exist12.

Clearly, the paper by Croft et al. doesn't answer all questions. But it greatly advances our understanding of why the vitamin-B12 requirements are so sporadic among the algae, and also points to an enticing variety of research opportunities.

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Andersen, R. Algae and the vitamin mosaic. Nature 438, 33–35 (2005). https://doi.org/10.1038/438033a

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