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DOE OSTI2021

In Vivo Entombment of Bacteria and Fungi during Calcium Oxalate, Brushite, and Struvite Urolithiasis

Human kidney stones form via repeated events of mineral precipitation, partial dissolution, and reprecipitation, which are directly analogous to similar processes in other natural and manmade environments, where resident microbiomes strongly influence biomineralization. High-resolution microscopy and high-fidelity metagenomic (microscopy-to-omics) analyses, applicable to all forms of biomineralization, have been applied to assemble definitive evidence of in vivo microbiome entombment during urolithiasis. Stone fragments were collected from a randomly chosen cohort of 20 patients using standard percutaneous nephrolithotomy (PCNL). Fourier transform infrared (FTIR) spectroscopy indicated that 18 of these patients were calcium oxalate (CaOx) stone formers, whereas one patient formed each formed brushite and struvite stones. This apportionment is consistent with global stone mineralogy distributions. Stone fragments from seven of these 20 patients (five CaOx, one brushite, and one struvite) were thin sectioned and analyzed using brightfield (BF), polarization (POL), confocal, super-resolution autofluorescence (SRAF), and Raman techniques. DNA from remaining fragments, grouped according to each of the 20 patients, were analyzed with amplicon sequencing of 16S rRNA gene sequences (V1–V3, V3–V5) and internal transcribed spacer (ITS1, ITS2) regions. Bulk-entombed DNA was sequenced from stone fragments in 11 of the 18 patients who formed CaOx stones, and the patients who formed brushite and struvite stones. These analyses confirmed the presence of an entombed low-diversity community of bacteria and fungi, including Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria, and Aspergillus niger. Bacterial cells approximately 1 μm in diameter were also optically observed to be entombed and well preserved in amorphous hydroxyapatite spherules and fans of needle-like crystals of brushite and struvite. In conclusion, these results indicate a microbiome is entombed during in vivo CaOx stone formation. Similar processes are implied for brushite and struvite stones. This evidence lays the groundwork for future in vitro and in vivo experimentation to determine how the microbiome may actively and/or passively influence kidney stone biomineralization.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems

It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling Bacteria is an uncultivated member of the Firmicutes phylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “ Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “ Candidatus Desulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific to these two environments.

Jungbluth, Sean P.↗

DOE OSTI2024

Staphylococcus aureus FtsZ and PBP4 bind to the conformationally dynamic N-terminal domain of GpsB

In the Firmicutes phylum, GpsB is a membrane associated protein that coordinates peptidoglycan synthesis with cell growth and division. Although GpsB has been studied in several bacteria, the structure, function, and interactome of Staphylococcus aureus GpsB is largely uncharacterized. To address this knowledge gap, we solved the crystal structure of the N-terminal domain of S. aureus GpsB, which adopts an atypical, asymmetric dimer, and demonstrates major conformational flexibility that can be mapped to a hinge region formed by a three-residue insertion exclusive to Staphylococci. When this three-residue insertion is excised, its thermal stability increases, and the mutant no longer produces a previously reported lethal phenotype when overexpressed in Bacillus subtilis. In S. aureus, we show that these hinge mutants are less functional and speculate that the conformational flexibility imparted by the hinge region may serve as a dynamic switch to fine-tune the function of the GpsB complex and/or to promote interaction with its various partners. Furthermore, we provide the first biochemical, biophysical, and crystallographic evidence that the N-terminal domain of GpsB binds not only PBP4, but also FtsZ, through a conserved recognition motif located on their C-termini, thus coupling peptidoglycan synthesis to cell division. Taken together, the unique structure of S. aureus GpsB and its direct interaction with FtsZ/PBP4 provide deeper insight into the central role of GpsB in S. aureus cell division.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Immediate impacts of soybean cover crop on bacterial community composition and diversity in soil under long-term Saccharum monoculture

Saccharum yield decline results from long-term monoculture practices. Changes in cropping management can improve soil health and productivity. Below-ground bacterial community diversity and composition across soybean (Glycine max (L.) Merr) cover crop, Saccharum monoculture (30+ year) and fallowed soil were determined. Near full length (~1,400 base pairs) of 16S rRNA gene sequences were extracted from the rhizospheres of sugarcane and soybean and fallowed soil were compared. Higher soil bacterial diversity was observed in the soybean cover crop than sugarcane monoculture across all measured indices (observed operationational taxonomic units, Chao1, Shannon, reciprocal Simpson and Jackknife). Acidocateria, Proteobacteria, Bacteroidetes and Planctomycetes were the most abundant bacterial phyla across the treatments. Indicator species analysis identified nine indicator phyla. Planctomycetes, Armatimonadetes and candidate phylum FBP were associated with soybean; Proteobacteria and Firmicutes were linked with sugarcane and Gemmatimonadetes, Nitrospirae, Rokubacteria and unclassified bacteria were associated with fallowed soil. Non-metric multidimensional scaling analysis showed distinct groupings of bacterial operational taxonomic units (97% identity) according to management system (soybean, sugarcane or fallow) indicating compositional differences among treatments. This is confirmed by the results of the multi-response permutation procedures (A = 0.541, p = 0.00045716). No correlation between soil parameters and bacterial community structure was observed according to Mantel test (r = 211865, p = 0.14). Use of soybean cover-crop fostered bacterial diversity and altered community structure. This indicates cover crops could have a restorative effect and potentially promote sustainability in long-term Saccharum production systems.

Bacterial diversity↗

DOE OSTI2020

Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites

“Higher” termites have been able to colonize all tropical and subtropical regions because of their ability to digest lignocellulose with the aid of their prokaryotic gut microbiota. Over the last decade, numerous studies based on 16S rRNA gene amplicon libraries have largely described both the taxonomy and structure of the prokaryotic communities associated with termite guts. Host diet and microenvironmental conditions have emerged as the main factors structuring the microbial assemblages in the different gut compartments. Additionally, these molecular inventories have revealed the existence of termite-specific clusters that indicate coevolutionary processes in numerous prokaryotic lineages. However, for lack of representative isolates, the functional role of most lineages remains unclear. We reconstructed 589 metagenome-assembled genomes (MAGs) from the different gut compartments of eight higher termite species that encompass 17 prokaryotic phyla. By iteratively building genome trees for each clade, we significantly improved the initial automated assignment, frequently up to the genus level. We recovered MAGs from most of the termite-specific clusters in the radiation of, for example, Planctomycetes, Fibrobacteres, Bacteroidetes, Euryarchaeota, Bathyarchaeota, Spirochaetes, Saccharibacteria, and Firmicutes, which to date contained only few or no representative genomes. Moreover, the MAGs included abundant members of the termite gut microbiota. This dataset represents the largest genomic resource for arthropod-associated microorganisms available to date and contributes substantially to populating the tree of life. More importantly, it provides a backbone for studying the metabolic potential of the termite gut microbiota, including the key members involved in carbon and nitrogen biogeochemical cycles, and important clues that may help cultivating representatives of these understudied clades.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Photosynthesis | The Heliobacteria

The heliobacteria are the only phototrophs in the Gram-positive group of bacteria. They are strict anaerobes that grow in a primarily fermentative mode in the dark. In the light, they use a homodimeric Type I photochemical reaction center to drive cyclic electron transport. They are unique in using the pigment bacteriochlorophyll g. All heliobacteria are unable to fix CO 2 but able to fix N2. Their core metabolism includes a complete TCA cycle with several reversible enzymes in common with the reverse (reductive) TCA cycle, but they lack an (ATP) citrate lyase that would allow CO 2 fixation. There are now several sequenced genomes available for different heliobacterial species, allowing hypotheses to be made concerning their metabolic potential. Here, techniques to introduce replicating plasmids into Heliobacterium modesticaldum, as well as leveraging its endogenous CRISPR/Cas system to edit its chromosome, have recently been pioneered, contributing to making this species a model system for this family.

59 BASIC BIOLOGICAL SCIENCES↗