Nature Communications

Abstract Conductive particles are common in coastal sediments, yet their role in shaping methane-producing communities and pathways remains unclear. We applied genome-resolved metagenomics to a sediment-derived consortium serially transferred for a decade and obligately dependent on granular activated carbon (GAC). We discovered a particle-obligate food web composed of electrogenic syntrophic acetate oxidizers (SAO), an electrotrophic methanogen, and necromass recyclers. The primary SAO electrogen, Candidatus Geosyntrophus acetoxidans, represents a new genus and possesses a complete acetate oxidation pathway and extracellular electron-transfer (EET) machinery, including two porin-cytochrome conduits, 43 additional multiheme cytochromes and conductive pili. A secondary SAO, a Lentimicrobium sp. with a giant PCC-cluster, supplies an alternative EET-linked acetate-oxidation route. Electrons from electrogens transfer via GAC to a Methanosarcina equipped with the heptaheme cytochrome MmcA and flagellin for electron uptake. These results provide a genomic blueprint of this particle-obligate environmental consortium and suggest an overlooked acetate-to-methane electron-transfer route in geoconductor-rich anoxic sediments.

Abstract Magnetoreception is a remarkable ability found across a diverse range of organisms, including bacteria, birds, fish, insects, and mammals, enabling them to detect and harness the Earth’s geomagnetic field. Recently, the recruitment of biomineralizing ectosymbionts by euglenozoans was evidenced as an ecological strategy for microeukaryotes to acquire this sense. Here, we report a case of magnetosymbiosis involving a ciliate and four populations of endosymbiotic bacteria experiencing genome reduction. Among these bacteria, one group of sulphate-reducing Desulfovibrionales was found to biomineralize bundles of bullet-shaped magnetite crystals. The ciliate’s magnetotaxis mirrors that of free-living magnetotactic bacteria and euglenozoans, enabling efficient navigation in chemically stratified aquatic environments. However, in this case, magnetotaxis arises from an endosymbiotic interaction. Using a combination of optical-, confocal-, electron- and X-ray-based microscopy techniques, together with genomic analyses, these findings demonstrate that magnetosymbiosis can emerge in unicellular eukaryotic lineages through endosymbiotic integration, expanding our understanding of such interactions in aquatic ecosystems. More broadly, this work contributes to the ongoing debate on the origins of magnetoreception in eukaryotes.

Abstract Segmented filamentous bacteria (SFB) describe morphologically similar gut commensals found in mammals, fish and birds. In mice, SFB intimately colonizes the ileal epithelium at the time of weaning and elicits a strong pleiotropic immune activation that fosters colonization resistance while augmenting disease severity in various disease models. SFB is therefore critical in both health and disease but information regarding SFB in humans remains limited. Here, we first identify and characterize a human SFB species with SFB-specific morphology, including the hook-like tip structure that mediates attachment, and unique genome features, including a starch and glycogen degradation module. This species, which we name Anisomitus miae and establish as the nomenclature type for the SFB genus, is common across Africa. We then bioinformatically identify, based on the 16S rRNA gene V3-V4 variable region sequence, four major, and two minor, human SFB lineages in forty-four countries distributed across all six inhabited continents. We provide evidence towards the co-colonization potential of the SFB lineages and their colonization dynamics, including a potent but short-lived colonization peak in children between one to five years of age. This study establishes the presence of multiple SFB species in the human population and SFB as a minor but wide-spread group of commensals in humans.

Abstract Model bacteria are fundamental for research, but knowledge about their ecology and evolution is often limited. Here, we establish an evolutionary and ecological context for the model organism Caulobacter crescentus —an alphaproteobacterium intensively studied for its dimorphic lifecycle. By analyzing the phylogenetic relatedness and genetic potential of hundreds of Caulobacterales species, we reveal substantial diversity regarding their environmental distribution, morphology, cell development, and metabolism. Our work provides insights into the evolutionary history of morphological features such as the cell curvature determinant crescentin and uncovers a striking case of convergent loss of traits for cellular dimorphism among close relatives of C. crescentus . Moreover, we find that genes for phototrophy are widespread across Caulobacterales and that the new genus Acaudatibacter , described here, includes the first reported Caulobacterales lineage with photoautotrophic potential. Our study advances our understanding of an environmentally widespread bacterial order and sheds light on the evolution of fundamental prokaryotic features.

Abstract Axenic cultures are essential for studying microbial ecology, evolution, and genomics. Despite the importance of pure cultures, public culture collections are biased towards fast-growing copiotrophs, while many abundant aquatic prokaryotes remain uncultured due to uncharacterized growth requirements and oligotrophic lifestyles. Here, we applied high-throughput dilution-to-extinction cultivation using defined media that mimic natural conditions to samples from 14 Central European lakes, yielding 627 axenic strains. These cultures include 15 genera among the 30 most abundant freshwater bacteria identified via metagenomics, collectively representing up to 72% of genera detected in the original samples (average 40%) and are widespread in freshwater systems globally. Genome-sequenced strains are closely related to metagenome-assembled genomes (MAGs) from the same samples, many of which remain undescribed. We propose a classification of several novel families, genera, and species, including many slowly growing, genome-streamlined oligotrophs that are notoriously underrepresented in public repositories. Our large-scale initiative to cultivate the “uncultivated microbial majority” has yielded a valuable collection of abundant freshwater microbes, characterized by diverse metabolic pathways and lifestyles. This culture collection includes promising candidates for oligotrophic model organisms, suitable for a wide array of ecological studies aimed at advancing our ecological and functional understanding of dominant, yet previously uncultured, taxa.

Abstract Numerous bacteria in the human gut microbiome remain unknown and/or have yet to be cultured. While collections of human gut bacteria have been published, few strains are accessible to the scientific community. We have therefore created a publicly available collection of bacterial strains isolated from the human gut. The Human intestinal Bacteria Collection (HiBC) ( https://www.hibc.rwth-aachen.de ) contains 340 strains representing 198 species within 29 families and 7 phyla, of which 29 previously unknown species are taxonomically described and named. These included two butyrate-producing species of Faecalibacterium and new dominant species associated with health and inflammatory bowel disease, Ruminococcoides intestinale and Blautia intestinihominis , respectively. Plasmids were prolific within the HiBC isolates, with almost half (46%) of strains containing plasmids, with a maximum of six within a strain. This included a broadly occurring plasmid (pBAC) that exists in three diverse forms across Bacteroidales species. Megaplasmids were identified within two strains, the pMMCAT megaplasmid is globally present within multiple Bacteroidales species. This collection of easily searchable and publicly available gut bacterial isolates will facilitate functional studies of the gut microbiome.