Comparative Analysis of Corrinoid Profiles across Host-Associated and Environmental Samples

Abstract

Vitamin B 12 (the cyanated form of cobalamin cofactors) is best known for its essential role in human health. In addition to its function in human metabolism, cobalamin also plays important roles in microbial metabolism and can impact microbial community function. Cobalamin is a member of the structurally diverse family of cofactors known as cobamides that are produced exclusively by certain prokaryotes. Cobamides are considered shared nutrients in microbial communities because the majority of bacteria that possess cobamide-dependent enzymes cannot synthesize cobamides de novo. Furthermore, different microbes have evolved metabolic specificity for particular cobamides, and therefore, the availability of cobamides in the environment is important for cobamide-dependent microbes. Determining the cobamides present in an environment of interest is essential for understanding microbial metabolic interactions. By examining the abundances of different cobamides in diverse environments, including 10 obtained in this study, we find that, contrary to its preeminence in human metabolism, cobalamin is relatively rare in many microbial habitats. Comparison of cobamide profiles of mammalian gastrointestinal samples and wood-feeding insects reveals that host-associated cobamide abundances vary and that fecal cobamide profiles differ from those of their host gastrointestinal tracts. Environmental cobamide profiles obtained from aquatic, soil, and contaminated groundwater samples reveal that the cobamide compositions of environmental samples are highly variable. As the only commercially available cobamide, cobalamin is routinely supplied during microbial culturing efforts. However, these findings suggest that cobamides specific to a given microbiome may yield greater insight into nutrient utilization and physiological processes that occur in these habitats.

Soil microbial community response to corrinoids is shaped by a natural reservoir of vitamin B12

“…5), though current methods do not allow us to separate cell-associated from extracellular corrinoids. Combined with our previous LC-MS results that showed approximately 95% of the corrinoid in soil collected from the same site is cobalamin [53], we estimate that the soil contained approximately 39 pmol cobalamin and 2 pmol 5-methylbenzimidazolylcobamide per gram. Based on an estimate of 10 9 microbial cells per gram of soil, this soil contains approximately 10 4 corrinoid molecules per microbial cell, a level sufficient to support maximal growth of bacteria in pure culture, and far above that required by corrinoid-dependent isolates obtained from this soil [14, 18, 54, 55].…”

“…These results could mean that much of the cobalamin detected in soil is bioavailable, and that cobalamin is not a limiting micronutrient in this environment. In nature, the introduction of corrinoids other than cobalamin to soil may mimic the interplay between soil fauna and microbes; the gut and fecal contents of several invertebrates and macrofauna have been found to contain diverse corrinoids that microbes may transiently encounter [53]. Indeed, we have observed that corrinoid-dependent taxa isolated from this soil are able to use many corrinoids undetected in this soil, with different affinities for each [18].…”

Phylogenetic distribution and experimental characterization of corrinoid production and dependence in soil bacterial isolates

“…Despite the presence of excess corrinoid in our isolation media, we recovered fewer corrinoid-dependent isolates than expected (26,57), which may be due to corrinoid-dependent bacteria having additional nutrient dependencies not satisfied by our isolation medium or requiring specific partners for their survival (6). Notably, all of the dependent isolates were able to use corrinoids that have not been detected in this soil (30).…”

“…1A), which has been shown to impact function – microbial preferences for particular corrinoid structures are apparent in their differential growth responses to corrinoids (17,29). Distinct groups of corrinoids have been detected in a variety of host-associated and environmental microbial communities, suggesting that microbes encounter diverse corrinoids in nature (30). Because most corrinoids are not commercially available, nearly all research on corrinoids has been performed only with B 12 (17).…”

Draft Genome Sequence ofPedococcussp. Strain 5OH_020 Isolated from California Grassland Soil

“…strain 5OH_020 was isolated from ungrazed grassland topsoil at the Hopland Research and Extension Center (39.00 N 123.08 W) by limiting dilution in methionine-dropout VL60 medium containing 0.1 g/L each of xylan, glucose, xylose, and N-acetyl glucosamine (1), amended with 10 nM 5-hydroxybenzimidazolyl cobamide ([5-OHBza]Cba) that we synthesized according to (2). [5-OHBza]Cba is a commercially-unavailable cobamide cofactor typically biosynthesized by methanogens and found in diverse environments such as animal gastrointestinal tracts and contaminated groundwater (3, 4, 5). To our knowledge, this is the first report of a bacterium isolated on a cobamide other than vitamin B 12 (cobalamin).…”