Lanthanide-Dependent Methylotrophs of the Family Beijerinckiaceae : Physiological and Genomic Insights

Abstract

Methylotrophic bacteria use methanol and related C1 compounds as carbon and energy sources. Methanol dehydrogenases are essential for methanol oxidation, while lanthanides are important cofactors of many pyrroloquinoline quinone-dependent methanol dehydrogenases and related alcohol dehydrogenases. We describe here the physiological and genomic characterization of newly isolated Beijerinckiaceae bacteria that rely on lanthanides for methanol oxidation. A broad physiological diversity was indicated by the ability to metabolize a wide range of multicarbon substrates, including various sugars, and organic acids, as well as diverse C1 substrates such as methylated amines and methylated sulfur compounds. Methanol oxidation was possible only in the presence of low-mass lanthanides (La, Ce, and Nd) at submicromolar concentrations (>100 nM). In a comparison with other Beijerinckiaceae, genomic and transcriptomic analyses revealed the usage of a glutathione- and tetrahydrofolate-dependent pathway for formaldehyde oxidation and channeling methyl groups into the serine cycle for carbon assimilation. Besides a single xoxF gene, we identified two additional genes for lanthanide-dependent alcohol dehydrogenases, including one coding for an ExaF-type alcohol dehydrogenase, which was so far not known in Beijerinckiaceae. Homologs for most of the gene products of the recently postulated gene cluster linked to lanthanide utilization and transport could be detected, but for now it remains unanswered how lanthanides are sensed and taken up by our strains. Studying physiological responses to lanthanides under nonmethylotrophic conditions in these isolates as well as other organisms is necessary to gain a more complete understanding of lanthanide-dependent metabolism as a whole. IMPORTANCE We supplemented knowledge of the broad metabolic diversity of the Beijerinckiaceae by characterizing new members of this family that rely on lanthanides for methanol oxidation and that possess additional lanthanide-dependent enzymes. Considering that lanthanides are critical resources for many modern applications and that recovering them is expensive and puts a heavy burden on the environment, lanthanide-dependent metabolism in microorganisms is an exploding field of research. Further research into how isolated Beijerinckiaceae and other microbes utilize lanthanides is needed to increase our understanding of lanthanide-dependent metabolism. The diversity and widespread occurrence of lanthanide-dependent enzymes make it likely that lanthanide utilization varies in different taxonomic groups and is dependent on the habitat of the microbes.

Extracellular and Intracellular Lanthanide Accumulation in the Methylotrophic Beijerinckiaceae Bacterium RH AL1

“…We did not detect a strong phosphorus signal in the EDX data of the identified lanthanide extorquens AM1 secretes a high-affinity, lanthanide-binding metallophore with a preference for lighter lanthanides (48). Strain RH AL1, isolated from acidic (pH 3.4-3.6) and metal-rich slags that contain bioavailable, lighter lanthanides (La, Ce, Nd; 27-64 ppm) (22), might be adapted and has a reduced need for a high-affinity lanthanide uptake system. Until now, we have no evidence that strain RH AL1 produces and secretes lanthanophores.…”

“…In the present study, we use the recently characterized Beijerinckiaceae bacterium RH AL1 (22) to win additional insights into lanthanide-dependent metabolism with a focus on lanthanide uptake and storage. Strain RH AL1 was isolated from earlyindustrial soft coal slags enriched in bioavailable lanthanides, possesses multiple lanthanide-dependent PQQ ADHs and lacks a Mxa-type MDH (22,23). We combined ultrathin section (TEM) and freeze-fracture transmission electron microscopy (FFTEM) with electron-dispersive X-ray spectroscopy (EDX) to study cultures grown with different lanthanum concentrations.…”

Methanogens and Their Syntrophic Partners Dominate Zones of Enhanced Magnetic Susceptibility at a Petroleum Contaminated Site

“…Paenibacillus strains have been frequently isolated from soil and they can degrade a variety of aliphatic and aromatic hydrocarbons (Grady et al, 2016). Despite considered being aerobic, the Alphaproteobacterium Beijerinckia was also a biomarker of the smear zone, and in addition to its ability to fix atmospheric nitrogen, it is able to oxidize a wide variety of organic compounds, including methane and methanol (Wegner et al, 2020).…”

Facultative methanotrophs – diversity, genetics, molecular ecology and biotechnological potential: a mini-review

“…These two strains were unable to grow on methanol in the absence of a rare-earth element, in common with a relatively small number of other methylotrophs [61, 77–79], which require these elements for methylotrophic growth. Subsequent to the isolation of these Xox-only Methylocella strains, additional methylotrophic (not methanotrophic) Xox-only members of the Beijerinckiaceae have been discovered [80]. Some of the facultative methanotrophs can grow on ethane or ethanol and so the identity of the enzyme(s) responsible for ethanol oxidation is of interest.…”