Ecology

Hydrochemistry and methane oxidation ratesThe water column of the deep North Basin is considered meromictic (i.e., permanently stratified). At the time of sampling for methane oxidation rate measurements in November 2016, the redox transition zone extended from 79 to 105 m depth; as defined here, with an upper boundary set at O2  More

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Ultra-small prokaryotes were prevalent across diverse aquifer lithologies and anoxic to oxic groundwatersWe used 16S rRNA gene amplicons to assess microbial community composition in 81 groundwater samples. Samples were collected from 59 wells over 10 aquifers in four geographic regions, separated by over a thousand kilometers, and encompassed wide-ranging aquifer chemistries and lithologies (Fig. 1a), comprising primarily shallow sandy-gravel aquifers, but also sand/silt, gravel/peat, volcanic (basalt, ignimbrite) and shell-bed aquifers (Table S1). A large portion of microbial community diversity comprised ultra-small groups of prokaryotes (Fig. 1b). Out of 52,553 OTUs, 21.8% (or 18.4% of 46,713 ASVs) were assigned to seven ultra-small microbial phyla (when considering CPR as the single Patescibacteria phylum). These comprised the bacterial phyla Patescibacteria and Dependentiae, and archaeal DPANN radiation. Altiarchaeota was included in DPANN as previously suggested [63, 64], although its taxonomic placement is uncertain due to genomic under-sampling [65, 66].Fig. 1: Distribution and abundance of ultra-small prokaryotes across groundwater sites.a Distribution of groundwater samples along DOC (0–26 g/m3), DO (0.37–7.5 g/m3) and nitrate-N (0.45–12.6 g/m3) concentrations scaled between 0 and 100. b Top plot: Richness of ultra-small prokaryote variants (rarefied ASVs) at each site. Middle plot: Proportion of ultra-small prokaryotes compared with the total microbial communities (black bars = OTUs, grey crosses = ASVs). Samples are ordered from least to most abundant. Lower plot: Phylum-level breakdown of amplicon based-relative abundance of Patescibacteria, Dependentiae and DPANN archaea (bottom). Symbol bars indicate aquifer lithology (top symbol bar), and oxygen content (lower symbol bar) with dark to light blue shading representing anoxic, suboxic, dysoxic to oxic groundwater. c Class-level rank abundance curve showing the average relative abundance of each genome across sites. The center line of each boxplot represents the median; the top and bottom lines are the first and third quartiles, respectively; and the whiskers show 1.5 times the interquartile range.Full size imageUltra-small prokaryotes were detected in all samples, regardless of lithology, chemistry or geography. They have also been reported from several aquifers and lithologies in the USA (sandy gravel, agriculturally-impacted river sediment, mixed marine sedimentary/metasedimentary rocks, plutonic rock, and sandstone [10, 18, 19, 22], and from a carbonate rock aquifer system in Germany [67, 68]. Collectively these findings demonstrate that ultra-small microorganisms are geographically widespread across diverse aquifer lithologies. Moreover, while ultra-small microorganisms have mostly been detected in anoxic environments [69,70,71,72] or cultivated under anoxic conditions [15, 25], we found representatives in all oxic groundwaters ( >3 mg/L DO) [73] (54/81 samples, Table S1). A few members of DPANN and Patescibacteria lineages have previously been detected in oxic environments [28, 67, 68, 74, 75], suggesting a degree of oxygen tolerance (genetic evidence presented below) or that these organisms are concentrated in anoxic niches within the aquifer substrate.The relative abundance of ultra-small microorganisms was highly variable across the studied aquifers, ranging from 0.04% to 22% of all bacterial and archaeal 16S rRNA gene sequences (7.2% average ±5.5% standard deviation; Fig. 1b). Samples with low relative abundances of ultra-small microorganisms (lower than the average) had overall lower alpha diversity (Shannon diversity indices and OTU or ASV richness) and were mostly from volcanic aquifer sites (Fig. 1b; Table S2). At the phylum level, Patescibacteria and Nanoarchaeota tended to dominate groundwater ultra-small communities (Fig. 1b). However, we found that ultra-small species level diversity overall was considerable with up to 1429 unique OTUs in a single groundwater sample (or up to 653 variants via the more conservative ASV method) (Table S2). Rarefaction curves show most variant diversity was captured across all samples, with curve slopes equaling zero (or approaching zero post rarefaction) (Fig. S1; Table S2). Finally, our results confirm the site specificity of ultra-small prokaryotes [10], with only 16 OTUs common across ≥50% of all 81 groundwater samples, or five ASVs across ≥20% of samples (three Parcubacteria, a Ca. Uhrbacteria, and a Woesearchaeales) (Table S2).High shared phylogenetic and genomic similarity to ultra-small prokaryotes from groundwaters elsewhereTo further assess the phylogeny and assess the genomic attributes and metabolic capacities of groundwater microbial communities, we reconstructed MAGs from 16 groundwater samples (eight wells over four sites and two aquifers). The dataset comprised 7,695 MAGs, including 539 unique MAGs ( >50% complete, 90% complete) (Table S3; Fig. S2). Based on phylogenetic analysis using GTDB [7, 76], MAGs represent 51 phyla, including five ultra-small microbial phyla (Table S3; Fig. S3). The ultra-small MAGs were found at all four sites and accounted for >1/3 of all unique MAGs (216 MAGs 50–100% complete, with 76 MAGs >90% complete). MAGs included 171 assigned to Patescibacteria, six to Dependentiae, and 39 to DPANN archaea (28 Nanoarchaeota, 10 Micrarchaeota, and one Altiarchaeota; Fig. 2a, b). The high representation of ultra-small prokaryotes in the MAG dataset further highlights the prevalence, diversity and abundance of these organisms in groundwater. Consistent with previous studies [6, 9, 77], genomes of ultra-small prokaryotes were small (1 ± 0.4 Mbp on average) with a tendency towards low GC contents (Figs. 3a, S2), and possessed limited metabolic capacities, which significantly differ between ultra-small bacterial and archaeal domains (results in Supplementary Materials; Figs. 3b, S2, S4).Fig. 2: Diversity of groundwater ultra-small microbial communities.Maximum likelihood phylogenetic trees of 177 unique ultra-small bacterial MAGs (a) and 39 unique ultra-small archaeal MAGs (b) recovered in this study. Outer rings indicate the site characteristics where MAGs were enriched. Enrichment factors were calculated as (average relative abundance in oxic and planktonic ultra-small microbial communities, respectively)/(average relative abundance in anoxic-to-dysoxic or sediment-enriched microbial communities, respectively). Trees are based on either 120 concatenated bacterial marker genes or 122 concatenated archaeal marker genes from GTDB-Tk, and were rooted to other groundwater bacterial and archaeal MAGs, respectively (Table S3). Scale bars indicate the number of substitutions per site. Branch background shading denotes Patescibacteria classes (clockwise): Gracilibacteria, Saccharimonadia, UBA1384, Dojkabacteria, Microgenomatia, Doudnabacteria, ABY1, Paceibacteria_A and Paceibacteria. c Proportion of ultra-small microbial OTUs (top) and MAGs (bottom) enriched in low and high oxygen groundwater, and in planktonic and sediment-enriched samples (Table S1). Enrichment factors were calculated as described above.Full size imageFig. 3: Estimated genome size, metabolic content and novelty of groundwater ultra-small prokaryotes.a Estimated genome size of groundwater MAGs calculated as (bin size – (bin size * contamination)) / (completeness), as described by Castelle et al. [9]. Genomes of ultra-small prokaryotes are colored by phylum-level. Other microbial genomes are shown in grey. b Principal Component Analysis (PCA) based on the composition of COG metabolic categories in recovered ultra-small MAGs. c (Right) Range of all pairwise AAI values (grey) and maximum AAI values (blue) between ultra-small prokaryote MAGs recovered in this study and GTDB representative genomes for a given phylum. Red dashed lines represent the AAI range defining the same family of organisms (45–65%) [74]. The number of genomes included in this analysis is indicated for each phylum in brackets. (Left) Proportion of ultra-small prokaryotic MAGs reconstructed in this study classified at each taxonomic level using GTDB-Tk.Full size imageCompared to reference genomes (GTDB species representatives), all recovered ultra-small MAGs are predicted to be novel species [78], and almost half were novel groundwater genera (Fig. 3c, results in Supplementary Materials). Most shared the highest affinity matches with other ultra-small genomes derived from aquifers elsewhere (e.g., in the USA), indicating niche adaptation within these lineages (although ultra-small MAGs from these groundwater ecosystems are over-represented in the GTDB database). Niche-specific phylogenetic conservation among geographically distant microorganisms in groundwater has likewise been reported among geographically distant anammox bacteria in groundwater [30].Ultra-small microbial communities were structured by geography, lithology, and dissolved oxygen concentrationsWhile ultra-small prokaryotes were ubiquitous in groundwater, and overall highly similar to those found in groundwater at different global locations, community compositions varied across sites. To investigate environmental factors (Table S1) influencing ultra-small community composition, we performed distance-based redundancy analysis (Fig. 4a). DO, pH, nitrate-N, sulfate, and DOC were significantly associated with differences in the distribution of 16S rRNA gene amplicon sequences annotated as Patescibacteria, Dependentiae and DPANN (permutation test, p  More

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