Into the darkness: the ecologies of novel ‘microbial dark matter’ phyla in an Antarctic lake

Abstract

Summary Uncultivated microbial clades (‘microbial dark matter’) are inferred to play important but uncharacterized roles in nutrient cycling. Using Antarctic lake (Ace Lake, Vestfold Hills) metagenomes, 12 metagenome‐assembled genomes (MAGs; 88%–100% complete) were generated for four ‘dark matter’ phyla: six MAGs from Candidatus Auribacterota (=Aureabacteria, SURF‐CP‐2), inferred to be hydrogen‐ and sulfide‐producing fermentative heterotrophs, with individual MAGs encoding bacterial microcompartments (BMCs), gas vesicles, and type IV pili; one MAG (100% complete) from Candidatus Hinthialibacterota (=OLB16), inferred to be a facultative anaerobe capable of dissimilatory nitrate reduction to ammonia, specialized for mineralization of complex organic matter (e.g. sulfated polysaccharides), and encoding BMCs, flagella, and Tad pili; three MAGs from Candidatus Electryoneota (=AABM5‐125‐24), previously reported to include facultative anaerobes capable of dissimilatory sulfate reduction, and here inferred to perform sulfite oxidation, reverse tricarboxylic acid cycle for autotrophy, and possess numerous proteolytic enzymes; two MAGs from Candidatus Lernaellota (=FEN‐1099), inferred to be capable of formate oxidation, amino acid fermentation, and possess numerous enzymes for protein and polysaccharide degradation. The presence of 16S rRNA gene sequences in public metagenome datasets (88%–100% identity) suggests these ‘dark matter’ phyla contribute to sulfur cycling, degradation of complex organic matter, ammonification and/or chemolithoautotrophic CO2 fixation in diverse global environments.

Discovery of a novel bacterial class with the capacity to drive sulfur cycling and microbiome structure in a paleo-ocean analog

“…Taxonomic a liation of the MAG using the genome classi er tool in the proGenomes database (900 000 genomes) resulted in no match, whereas phylogenetic analyses of the MAG using GTDB-tk pipeline [34] revealed deep branching within the Fibrobacterota, Chlorobiota and Bacteroidota (FCB) group, basal to Zixibacteria and Calditrichota phyla and within the "AABM5-125-24" phylum (Figure 2). A few members of the AABM5-125-24 phylum, also named Candidatus Electryoneota [40] have been identi ed as rare members of Ace Lake, Antarctica [17], which is a meromictic marine-derived lake like Lake A. However, analysis of the average amino acid identity (AAI, Figure 3) indicated a low similarity with most of Electryoneota/AABM5-125-24 genomes (<46%), including the Ace Lake representatives and a maximum of 57.5% of amino acid identity percentage with a genome recovered from Black Sea brackish waters (Figure 2).…”

“…However, structure of the operon, and more particularly the genes involved in electron transfer were variable, and included, in two other MAGs, genes coding the cytochrome b 6 f instead of dsrJOP. In addition to the potential for sulfate reduction, previous studies on Electryoneota lineages have reported a potential capability for aerobic respiration using high a nity cytochromes (cbb3-type) and sul de oxidation genes, suggesting a facultative anaerobic lifestyle [17]. None of these aerobic pathways were detected in the Tariuqbacter genome, suggesting a strictly anaerobic metabolism that differs from Antarctic Electryoneota lineages.…”

“…Extreme environments, such as hydrothermal vents [13][14][15], hypersaline basins [16], deep underground aquifers [3] and polar lakes [17] are major sources of previously unknown microbial biodiversity and are useful systems to investigate limits of life, microbial biogeography and distribution of lineages in nature [18]. High Arctic Lake A (latitude 83°N) is one of the northernmost lakes of the world and has many extreme features.…”

Population structure of an Antarctic aquatic cyanobacterium

“…GC content-read depth analysis was performed as described previously for Haloarchaea [39] and Ca. Chlorobium antarcticum [29].…”

“…Expeditions to retrieve samples from Ace Lake for metaproteogenomics first occurred in the austral summer 2006/2007, and subsequently in 2008/2009, with samples covering a complete seasonal cycle obtained in 2013-2015; biomass was collected by sequential size fractionation onto 3.0-, 0.8-and 0.1-μm pore-sized filters, with the metagenome data generated enabling the characterisation of diverse lake microorganisms [24,25,28,29,38,39]. The abundance of Synechococcus-like operational taxonomic units (OTUs) was assessed according to filter fraction, lake depth and season (Fig.…”