Amann, Rudolf I

Abstract Ferdinand Cohn observed abundant filamentous bacteria in drinking water wells in 1870 that he named Crenothrix polyspora. Subsequent research has revealed the methanotrophic metabolism of Crenothrix bacteria and their disproportionately high activity in stratified lakes compared to unicellular methanotrophs, yet laboratory cultivation has proven elusive, leaving the ecophysiology of Crenothrix bacteria largely unknown. Here we report the isolation of two methanotrophic strains of the “lacustrine Crenothrix” clade from an iron-rich wetland and reveal their unique cell biology and ecology. We demonstrate that the strains are microaerobic and grow as filaments of cells, which are connected by unidirectionally oriented structures. The strains have broad genomic repertoires for addressing O2 limitation that are uniquely associated with lacustrine Crenothrix compared to related clades based on genome data. Aligning with laboratory observations, we identify lacustrine Crenothrix bacteria along potential redox gradients in the wetland at iron-rich snow sites, and we also detect such bacteria in diverse global ecosystems based on public metagenome searches. Together, our data strongly point to an ecophysiology of lacustrine Crenothrix bacteria that is tightly linked to O2 limitation, and we propose that the strains uniquely store or share metabolic intermediates between cells in filaments to thrive under such conditions. Our cultivation-based findings for these strains, which we name Allocrenothrix methanica, provide new insights into the diversity, evolution, and ecology of filamentous methanotrophs, connecting over 150 years of microbiology research and opening vast new opportunities to investigate bacteria contributing to the global methane cycle under O2 limitation.

Abstract Marine algae annually sequester petagrams of carbon dioxide into polysaccharides, which are a central metabolic fuel for marine carbon cycling. Diatom microalgae produce sulfated polysaccharides containing methyl pentoses that are challenging to degrade for bacteria compared to other monomers, implicating these sugars as a potential carbon sink. Free-living bacteria occurring in phytoplankton blooms that specialise on consuming microalgal sugars, containing fucose and rhamnose remain unknown. Here, genomic and proteomic data indicate that small, coccoid, free-living Verrucomicrobiota specialise in fucose and rhamnose consumption during spring algal blooms in the North Sea. Verrucomicrobiota cell abundance was coupled with the algae bloom onset and accounted for up to 8% of the bacterioplankton. Glycoside hydrolases, sulfatases, and bacterial microcompartments, critical proteins for the consumption of fucosylated and sulfated polysaccharides, were actively expressed during consecutive spring bloom events. These specialised pathways were assigned to novel and discrete candidate species of the Akkermansiaceae and Puniceicoccaceae families, which we here describe as Candidatus Mariakkermansia forsetii and Candidatus Fucivorax forsetii. Moreover, our results suggest specialised metabolic pathways could determine the fate of complex polysaccharides consumed during algae blooms. Thus the sequestration of phytoplankton organic matter via methyl pentose sugars likely depend on the activity of specialised Verrucomicrobiota populations.