Lanthanide-dependent methylotrophy in Beijerinckiaceae
What comes to your mind when you think about lanthanides aka rare earth elements? We all carry them around in our smartphones, and you might know that industry needs them for numerous high-tech products including optical glas, superconductors, and batteries (Figure 1). Maybe you also know that China produces most of them - demands are high and global production is limited.
While it was hypothesized for years that lanthanides would be powerful enzymatic co-factors due to their strong Lewis acidity, lanthanide-dependent enzymes were only discovered a few years ago in methylotrophic bacteria. Lanthanides are the most recently described life metals. The relevance of lanthanides goes beyond mcirobiology as positive effects of lanthanides on crop growing and livestock are known for a long time, while the underlying mechanisms are not understood.
In methylotrophic bacteria lanthanides function as co-factors in methanol dehydrogenase, the key enzyme of methanol oxidation. Taking into account the ecological role of methylotrophs, lanthanides are of high relevance with respect to microbial carbon cycling.
Figure 1: The roles of lanthanides. Lanthanides are needed for many high-tech applications. In the context of microbiology, lanthanides are primarily known from methylotrophic bacteria, which need them as enzymatic co-factors for methanol oxidation - a process highly relevant for global carbon cycling. The ability to solubilize lanthanides makes methylotrophs an attractive target for the biologically mediated recovery of lanthanides.
The ability of certain methylotrophic taxa to solubilize lanthanides facilitates the development of methods to recover these valuable metals biologically for instance by coupling lanthanide enrichment to the consumption of waste and inexpensive feedstocks such as methane and methanol.
Research dedicated to lanthanide-dependent metabolism is severely limited to few model organisms that do not represent the taxonomic and expected functional diversity of microbes utilizing lanthanides. I'm working on establishing a new, lanthanide-dependent methylotroph of the family Beijerinckiaceae, strain AL1 (Figure 2), as platform to win a more comprehensive understanding about lanthanide-dependent metabolism (Wegner et al., 2020). Strain AL1 was isolated from soft coal slags enriched in lanthanides (Wegner and Liesack, 2017) and in comparison to methylotrophic model organisms it only posseses lanthanide-dependent methanol dehydrogenases and multiple other lanthanide-dependent enzymes with unknown substrate spectra. Recently, we could show periplasmic storage of lanthanides in strain AL1, something that was so far not seen in other methylotrophs (Figure 3).
Figure 2: A phylogenomic tree of the family Beijerinckiaceae. Phylogenomic analyses of Beijerinckiaceae strains isolated from early-industrial soft coal slags was done based on sequenced genomes and available genomes of related family members using a set of genes representing the core genome of the family Beijerinckiaceae. Phylogenomics revealed a distinct grouping of the isolated strains, and calculated percentages of conserved proteins revealed that the isolated strains constitute a new genus-level group (modified based on Wegner et al., 2020).
Figure 3: Freeze-fracture TEM image of strain AL1. Growing strain AL1 at 1 and 10 µM revealed extracellular storage of lanthanides attached to outer membrane vesicle-like material. A closer look with freeze-fracture TEM also identified intracellular storage in the periplasm. The black arrow indicates an intracellular lanthanum deposit. PF = protoplasmic fracture face, CM = cytoplasmic membrane, OM = outer membrane, PP = periplasm (modified based on Wegner et al., 2021).
Wegner CE, M Westermann, F Steiniger, L Gorniak, R Budhraja, L Adrian, K Küsel (2021). Extracellular and intracellular lanthanide accumulation in the methylotroph Beijerinckiaceae bacterium RH AL1. Appl. Environ. Microbiol. 87: e03144-20. 10.1128/AEM.03144-20
Wegner CE, Gorniak L, Riedel S, Westermann M, Küsel K (2020) Lanthanide-Dependent Methylotrophs of the Family Beijerinckiaceae: Physiological and Genomic Insights. Appl. Environ. Microbiol. 86: e01830-19 doi:10.1128/AEM.01830-19
Wegner CE, Liesack W (2017) Unexpected dominance of elusive Acidobacteria in early industrial soft coal slags. Front. Microbiol. 8:1023 doi: 10.3389/fmicb.2017.01023
Complex organic matter breakdown and carbon cycling in wetlands
Methane is a major driver of global climate change and it is a product of anaerobic organic matter breakdown. A significant proportion of anthropogenic methane is emitted from (artificial) wetlands, including rice paddies. Microbes in wetlands are commonly exposed to recalcitrant organic carbon in form of complex polysaccharides and lignins. Methane emissions from wetlands are rate-limited by the breakdown of these carbon sources (Figure 4). The enzymatic toolkit needed for breaking down these carbon sources and the microbes possessing them are highly diverse.
Considering the ongoing advance of global climate change, methane emissions from wetlands are expected to increase as so far buried organic carbon becomes more prone to breakdown. The only known sink of atmospheric methane and C1 compounds contributing to methane emissions are methanotrophic/methylotrophic prokaryotes, which makes them a prime target to learn more about natural mechanisms of methane mitigation.
Figure 4: Anaerobic breakdown of complex organic matter by methanogenic communities. Dependent on the environment, terrestrial versus aquatic, complex organic matter originates from different sources. Complex organic matter is almost exclusively a result of biomass assimilation. Except for methanogenesis, all breakdown steps can occur under oxic and anoxic conditions. Fermenting organisms hydrolyse and ferment biopolymers to primary and secondary fermentation products,which are subsequently syntrophically converted to H2/CO2 and acetate. Acetate and H2/CO2 represent the two major substrate pools for methanogenesis.
Past and ongoing research of mine is driven by the goal of learning more about complex carbon turnover in artificial and natural wetlands. A more recent aspect of this research is the effect of environmental stress (salt stress, draught) on complex organic carbon turnover. Moreover, I'm interested in methylotrophs/methanotrophs from environments exposed to naturally high methane concentrations (e.g. the surrounding of methane seeps, Figure 5), and extreme environments in general to learn more about underlying mechanisms of C1 carbon turnover.
Figure 5: Terrestrial methane seepage. Geological methane originates from sources including coal beds and gas deposits. Methane reservoirs are usually trapped under compacted layers of rock. A release into the atmosphere is possible through small cracks, which arise, for instance, through the retreat of glaciers and thawing permafrost. Methane seeps are diverse, and among other structures, include small gas vents (microseeps) and mud volcanoes (macroseeps).
Wu X, Liu P, Wegner CE, Luo Y, Xiao K-Q, Cui Z, Zhang F, Liesack W, Peng J (2021) Deciphering microbial mechanism underlying soil organic carbon storage in a wheat maize rotation system. Sci. Total Environ. (accepted) 10.1016/j.scitotenv.2021.147798
Abdallah RZ, Wegner CE, Liesack W (2019) Community transcriptomics reveals drainage effects on paddy soil microbiome across all three domains of life. Soil Biol. Biochem. 132:131-142 doi: doi.org/10.1016/j.soilbio.2019.01.023
Peng J, Wegner CE, Bei Q, Liu P, Liesack W (2018) Metatranscriptomics reveals a different temperature effect on the structural and functional organization of the anaerobic food web in rice field soil. Microbiome 6:169 doi: 10.1186/s40168-018-0546-9
Peng J, Wegner CE, Liesack W (2017) Short-term exposure of paddy soil microbial communities to salt stress triggers different transcriptional responses of key taxonomic groups. Front. Microbiol. 8:400 doi: 10.3389/fmicb.2017.00400
Ivanova AA, Wegner CE, Kim Y, Liesack W, Dedysh SN (2016) Identification of microbial populations driving biopolymer degradation in acidic peatlands by metatranscriptomic analysis. Mol. Ecol. 19:4818-4835 doi: 10.1111/mec.13806
Wegner CE, Liesack W (2016) Microbial community dynamics during the early stages of plant polymer breakdown in paddy soil. Environ. Microbiol. 18: 2825-2842 doi: 10.1111/1462-2920.12815
Oshkin IY, Wegner CE, Lüke C, Glagolev MV, Filippov IV, Pimenov NV, Liesack W, Dedysh SN (2014) Gammaproteobacterial methanotrophs dominate cold methane seeps in floodplains of Western Siberian Rivers. Appl. Environ. Microbiol. 80: 5944-5954 doi: 10.1128/AEM.01539-14