Publications

3819

Abstract  The Gemmatimonadota phylum has been widely detected in diverse natural environments, yet their specific ecological roles in many habitats remain poorly investigated. Similarly, the Candidatus ARS69 phylum has been identified only in a few habitats, and literature on their metabolic functions is relatively scarce. In the present study, we investigated the ecological significance of phyla Ca. ARS69 and Gemmatimonadota in the Arctic glacier foreland (GF) ecosystems through genome-resolved metagenomics. We have reconstructed the first high-quality metagenome-assembled genome (MAG) belonging to Ca. ARS69 and 12 other MAGs belonging to phylum Gemmatimonadota from the three different Arctic GF samples. We further elucidated these two groups phylogenetic lineage and their metabolic function through phylogenomic and pangenomic analysis. The analysis showed that all the reconstructed MAGs potentially belonged to novel species. The MAGs belonged to Ca. ARS69 consist about 8296 gene clusters, of which only about 8% of single-copy core genes (n = 980) were shared among them. The study also revealed the potential ecological role of Ca. ARS69 is associated with carbon fixation, denitrification, sulfite oxidation, and reduction biochemical processes in the GF ecosystems. Similarly, the study demonstrates the widespread distribution of different classes of Gemmatimonadota across wide ranges of ecosystems and their metabolic functions, including in the polar region. Key points • Glacier foreland ecosystems act as a natural laboratory to study microbial community structure. • We have reconstructed 13 metagenome-assembled genomes from the soil samples. • All the reconstructed MAGs belonged to novel species with different metabolic processes. • Ca. ARS69 and Gemmatimonadota MAGs were found to participate in carbon fixation and denitrification processes.

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.