Over the past several years, I have been asking random people whether they knew what lanthanides (Ln) were. Their answers were sometimes surprising. For example, a scientist friend of mine (to his credit, he is not a chemist) said he never heard of them (and this is a typical layperson answer). However, a massage therapist I randomly questioned said absolutely, I know what they are. When further queried as to how and why, she explained she has learned in her homeopathic course. Indeed, not only internet blogs but entire books have been published on the beneficial effects of Ln on humans. Is this true? If yes, is this the humans themselves or human microbiomes that might be positively responding to Ln? There is little scientific literature supporting effects of Ln on humans. However, beneficial effects of Ln on (agricultural) plants have been well documented. Once again, it is not clear whether the plant itself or plant microbiome benefits from the presence of Ln.
Much more concrete data are now available for bacteria. Methylotrophic bacteria, the ones that can consume simple and abundant chemicals such as methane or methanol, were the first to be demonstrated to incorporate Ln into the active site of a special enzyme, XoxF that is a methanol dehydrogenase (MDH). This enzyme is very similar to its calcium (Ca)-dependent counterpart, MxaFI, discovered and characterized decades before. Are Ln metals unique to the methylotrophs then? Not really, as at least one non-methylotroph, a Pseudomonas, has been previously identified that relies on Ln to metabolize a range of volatile alcohols.
The questions we wanted to address in our recent study were: (1) is Ln-based biochemistry rare in microbes? (2) if not, do Ln enzymes from methylotrophs and beyond display similar biochemical properties? and, (3) are Ln enzymes strictly reliant on Ln, or could they possibly possess broader metal specificities?
Through simple bioinformatic analyses, we demonstrate that Ln enzymes appear to be broadly occurring among bacteria, including some of the globally distributed, numerically abundant and environmentally important species. We then employ synthetic biology to generate genes for and to physiologically express putative Ln enzymes from bacteria representing some of these guilds, including the phylogenetically disparate rhizobia, playing an important role as dinitrogen-fixing plant symbionts, members of Vibrionales, known for parasitic relationships with multiple species, and the metabolically versatile Rhodobacterales and Rhodospirillales, abundant in world oceans. Through these analyses, we uncover a range of biochemical parameters, providing a solid database for comparative analysis for Ln enzymes characterized in the future. As most of the enzymes we characterized reveal high affinity for methanol, we reconstruct potential methylotrophy pathways in the bacterial guilds not known fir this capability. The presence of these pathways suggests that methylotrophy is much more widespread in the microbial world than previously appreciated. Importantly, as the new dogma has been emerging recently, of the strict reliance of alternative MDH enzymes on either Ln or Ca, we demonstrate that enzymes may be promiscuous in their metal specificity, revealing activity with both Ln and Ca. With these data in hand, we are closer to resolving the questions pertinent to the potential role of Ln in plant and animal health. Full text of this article has been published in the ISME Journal (Huang et al 2019).
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