Publications

4876

ABSTRACT The unique cell biology presented by members of the phylum Planctomycetota has puzzled researchers ever since their discovery. Initially thought to have eukaryotic-like features, their traits are now recognized as exceptional but distinctly bacterial. However, recently discovered strains again added novel and stunning aspects to the planctomycetal cell biology—shapeshifting by members of the “ Saltatorellus ” clade to an extent that is unprecedented in any other bacterial phylum, and phagocytosis-like cell engulfment in the bacterium “ Candidatus Uabimicrobium amorphum.” These recent additions to the phylum Planctomycetota indicate hitherto unexplored members with unique cell biology, which we aimed to make accessible for further investigations. Targeting bacteria with features like “ Ca. U. amorphum”, we first studied both the morphology and behavior of this microorganism in more detail. While similar to eukaryotic amoeboid organisms at first sight, we found “ Ca. U. amorphum” to be rather distinct in many regards. Presenting a detailed description of “ Ca. U. amorphum,” we furthermore found this organism to divide in a fashion that has never been described in any other organism. Employing the obtained knowledge, we isolated a second “bacterium of prey” from the harbor of Heligoland Island (North Sea, Germany). Our isolate shares key features with “ Ca. U. amorphum”: phagocytosis-like cell engulfment, surface-dependent motility, and the same novel mode of cell division. Being related to “ Ca. U. amorphum” within genus thresholds, we propose the name “ Ca. Uabimicrobium helgolandensis” for this strain. IMPORTANCE “ Candidatus Uabimicrobium helgolandensis” HlEnr_7 adds to the explored bacterial biodiversity with its phagocytosis-like uptake of prey bacteria. Enrichment of this strain indicates that there might be “impossible” microbes out there, missed by metagenomic analyses. Such organisms have the potential to challenge our understanding of nature. For example, the origin of eukaryotes remains enigmatic, with a contentious debate surrounding both the mitochondrial host entity and the moment of uptake. Currently, favored models involve a proteobacterium as the mitochondrial progenitor and an Asgard archaeon as the fusion partner. Models in which a eukaryotic ancestor engulfed the mitochondrial ancestor via phagocytosis had been largely rejected due to bioenergetic constraints. Thus, the phagocytosis-like abilities of planctomycetal bacteria might influence the debate, demonstrating that prey engulfment is possible in a prokaryotic cellular framework.

AbstractThe continental bedrock contains groundwater-bearing fractures that are home to microbial populations that are vital in mediating the Earth’s biogeochemical cycles. However, their diversity is poorly understood due to the difficulty of obtaining samples from this environment. Here, a groundwater-bearing fracture at 975 m depth was isolated by employing packers in order to characterize the microbial community via metagenomes combined with prokaryotic and eukaryotic marker genes (16S and 18S ribosomal RNA gene). Genome-resolved analyses revealed a community dominated by sulfate-reducing Bacillota, predominantly represented by Candidatus Desulforudis audaxviator and with Wood-Ljungdahl as the most prevalent pathway for inorganic carbon fixation. Moreover, the eukaryotic community had a considerable diversity and was comprised of mainly flatworms, chlorophytes, crustaceans, ochrophytes, and fungi. These findings support the important role of the Bacillota, with the sulfate reducer Candidatus Desulforudis audaxviator as its main representative, as primary producers in the often energy-limited groundwaters of the continental subsurface.

Phytoplasmas are obligate intracellular pathogens that profoundly modify the development, physiology and behavior of their hosts by secreting effector proteins that disturb signal pathways and interactions both in plant and insect hosts. The characterization of effectors and their host-cell targets was performed for only a few phytoplasma species where it was shown that the SAP11 effector alters plant morphology by destabilizing plant transcription factors: TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCPs). To explore the possible role of the SAP11-like effector from ‘Ca. P. solani’, we used Arabidopsis thaliana as a model plant. The SAP11-like effector gene from ‘Ca. P. solani’ was introduced into arabidopsis by floral dip and transgenic lines were regenerated. In planta bimolecular fluorescence complementation (BIFC) assays in agroinfiltrated Nicotiana benthamiana leaf cells were conducted to detect interactions between SAP11-like and AtTCP2 and AtTCP4 using confocal microscopy. SAP11-like from ‘Ca. P. solani’ induced significant phenotypic changes in arabidopsis, including crinkled leaves with reduced size, lower biomass, more axillary branches, changes in root morphology, and crinkled and smaller siliques. The BIFC assays proved in planta interaction of SAP11-like effector with AtTCP2 and AtTCP4. To our knowledge, this is the first characterization of the interaction between the ‘Ca. P. solani’ effector and plant transcription factors, suggesting a potential mechanism of modulating plant development and induction of characteristic symptoms in ‘Ca. P. solani’-infected plants.

Abstract Vitamin B1 is a universally required coenzyme in carbon metabolism. However, most marine microorganisms lack the complete biosynthetic pathway for this compound and must acquire thiamin, or precursor molecules, from the dissolved pool. The most common version of Vitamin B1 auxotrophy is for thiamin's pyrimidine precursor moiety, 4‐amino‐5‐hydroxymethyl‐2‐methylpyrimidine (HMP). Frequent HMP auxotrophy in plankton and vanishingly low dissolved concentrations (approximately 0.1–50 pM) suggest that high‐affinity HMP uptake systems are responsible for maintaining low ambient HMP concentrations. We used tritium‐labelled HMP to investigate HMP uptake mechanisms and kinetics in cell cultures of Candidatus Pelagibacter st. HTCC7211, a representative of the globally distributed and highly abundant SAR11 clade. A single protein, the sodium solute symporter ThiV, which is conserved across SAR11 genomes, is the likely candidate for HMP transport. Experimental evidence indicated transport specificity for HMP and mechanistically complex, high‐affinity HMP uptake kinetics. Km values ranged from 9.5 pM to 1.2 nM and were dramatically lower when cells were supplied with a carbon source. These results suggest that HMP uptake in HTCC7211 is subject to complex regulation and point to a strategy for high‐affinity uptake of this essential growth factor that can explain natural HMP levels in seawater.

AbstractGut microbiota dysbiosis has been implicated in rheumatoid arthritis (RA) and influences disease progression. Although molecular and culture‐independent studies revealed RA patients harbored a core microbiome and had characteristic bacterial species, the lack of cultured bacterial strains had limited investigations on their functions. This study aimed to establish an RA‐originated gut microbial biobank (RAGMB) that covers and further to correlates and validates core microbial species on clinically used and diagnostic inflammation and immune indices. We obtained 3200 bacterial isolates from fecal samples of 20 RA patients with seven improved and 11 traditional bacterial cultivation methods. These isolates were phylogenetically identified and selected for RAGMB. The RAGMB harbored 601 bacterial strains that represented 280 species (including 43 novel species) of seven bacterial phyla. The RAGMB covered 93.2% at species level of medium‐ and high‐abundant (relative abundances ≥0.2%) RA gut microbes, and included four rare species of the phylum Synergistota. The RA core gut microbiome was defined and composed of 20 bacterial species. Among these, Mediterraneibacter tenuis and Eubacterium rectale were two species that statistically and significantly correlated with clinically used diagnostic indices such as erythrocyte sedimentation rate (ESR) and IL‐10. Thus, M. tenuis and E. rectale were selected for experimental validation using DSS‐treated and not DSS‐treated mice model. Results demonstrated both M. tenuis and E. rectale exacerbated host inflammatory responses, including shortened colon length and increased spleen weight, decreased IL‐10 and increased IL‐17A levels in plasma. Overall, we established the RAGMB, defined the RA core microbiome, correlated and demonstrated core microbial species effected on host inflammatory and immune responses. This work provides diverse gut microbial resources for future studies on RA etiology and potential new targets for new biomedical practices.

AbstractCulture collections such as the Blue Biotechnology and Ecotoxicology Culture Collection (LEGE‐CC) hold approximately 1200 cyanobacterial strains and are critical community resources. However, many isolates in this and other collections have not been described with a polyphasic approach, and this limits further study. Here, we employed a polyphasic methodology that integrates 16S rRNA gene phylogenetic analyses, similarity (p‐distance), 16S‐23S ITS rRNA region secondary structures, morphological analyses, and habitat assessments to describe four novel cyanobacterial genera from the LEGE‐CC, Portugal. Pseudolimnococcus planktonicus gen. et sp. nov. (Chroococcales) is phylogenetically and morphologically related to Limnococcus. The 16S rRNA gene similarity between the types of both genera is only 93.1%. Morphologically, Pseudolimnococcus cells do not reach the original spherical shape before the next division or have aerotopes and firm mucilage, while Limnococcus cells reach the original shape, lack aerotopes, and have diffluent mucilage. Eucapsopsis lusitanus gen. et sp. nov. (Chroococcales) is morphologically similar to Eucapsis but differs from it by having aerotopes and diffluent envelope. Eucapsis lacks aerotopes and has firm mucilaginous envelopes, rarely diffluent. Both genera are phylogenetically very distant from each other and have only 90.68% 16S rRNA gene similarity. Pseudoacaryochloris arrabidensis gen. et sp. nov. (Acaryochloridales) differs from Acaryochloris by the lack of mucilaginous envelope, which is present in Acaryochloris. Both genera are phylogenetically distant and have only 94.1% 16S rRNA gene similarity. Moreover, Acaryochloris is marine (sponge symbiont), while Pseudoacaryochloris is from freshwater. Vasconcelosia minhoensis gen. et sp. nov. (Nodosilineales) is phylogenetically related to Cymatolege but has only 94.3% similarity with this genus. Morphologically both genera are distinct. Vasconcelosia has a Romeria‐like structure, while Cymatolege has a Phormidium‐like structure. In all cases the 16S‐23S ITS rRNA region secondary structures are in agreement with the other analyses. These novel genera expand the diversity of cyanobacteria in culture collections.