Abstract

Members of the candidate phylum Acetothermia are globally distributed and detected in various habitats. However, little is known about their physiology and ecological importance. In this study, an operational taxonomic unit belonging to Acetothermia was detected at high abundance in four full-scale anaerobic digesters by 16S rRNA gene amplicon sequencing. The first closed genome from this phylum was obtained by differential coverage binning of metagenomes and scaffolding with long nanopore reads. Genome annotation and metabolic reconstruction suggested an anaerobic chemoheterotrophic lifestyle in which the bacterium obtains energy and carbon via fermentation of peptides, amino acids, and simple sugars to acetate, formate, and hydrogen. The morphology was unusual and composed of a central rod-shaped cell with bipolar prosthecae as revealed by fluorescence in situ hybridization combined with confocal laser scanning microscopy, Raman microspectroscopy, and atomic force microscopy. We hypothesize that these prosthecae allow for increased nutrient uptake by greatly expanding the cell surface area, providing a competitive advantage under nutrient-limited conditions.

Highlights

  • Microorganisms drive the major biogeochemical nutrient cycles, which are fundamental for many biotechnological processes and directly linked to our health [1,2,3]

  • Acetothermia bacteria have previously been observed in anaerobic digesters [34], but their distribution and abundance in these systems are not known

  • A single operational taxonomic unit (OTU) assigned to phylum Acetothermia was observed in four mesophilic sludge digesters at two wastewater treatment plants (WWTPs) from the survey of 31 digesters (Fig. 1a)

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Summary

Introduction

Microorganisms drive the major biogeochemical nutrient cycles, which are fundamental for many biotechnological processes and directly linked to our health [1,2,3]. Cultureindependent surveys of bacterial communities based on amplicon sequencing of 16S rRNA genes or concatenated single-copy phylogenetic marker genes have revolutionized our understanding of microbial community dynamics and diversity [3,4,5,6]. The fast developments in next-generation sequencing and metagenomics enable the characterization of the whole community gene pool and can be used to elucidate the functional potential of individual microbial members This allows us to better understand the ecological roles and interactions of the ubiquitous uncultivated microorganisms [13,14,15,16]. Such attempts have been made to establish metabolic models and predict the ecophysiology of several candidate bacteria, such as Candidatus Fermentibacter daniensis (candidate phylum Hyd24-12) [17], OP9/ JS1 (candidate phylum Atribacteria) [18], and Candidatus Promineofilum breve (phylum Chloroflexi) [19]

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