Genome-resolved metagenomics reveals site-specific diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems

He, Christine; Keren, Ray; Whittaker, Michael; Farag, Ibrahim; Doudna, Jennifer A.; Cate, Jamie H. D.; Banfield, Jillian F.

doi:10.1038/s41564-020-00840-5

Cited by 146 publications

(196 citation statements)

References 88 publications

(145 reference statements)

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“…Patescibacteria with an average relative abundance of 50% across all wells and a maximum of 79% in the 0.1 µm filter fraction. Compared to other groundwater communities dominated by CPR bacteria ranging from 2-28% [16], 3-40% [18], 10-28% [7] and 36-65% [15], the exceptionally high abundance of CPR bacteria discovered in this study is distributed over distinct geochemical zones spanning oxic and anoxic conditions [17,33].…”

Section: Discussionmentioning

confidence: 49%

“…with Paramecium bursaria, a ciliated protist in freshwater [26], or with Actinobacteria (Actinomyces odontolyticus, Propionibacterium propionicus, Schaalia meyeri) in the human oral cavity [12,[27][28][29]. Similarly, CPR bacteria attach as episymbionts to putative bacterial hosts through pilin-like appendages in pristine groundwater [18].…”

Section: Introductionmentioning

confidence: 99%

“…Patescibacteria, initially recovered from groundwater and aquatic sediments [2,3], are now shown to inhabit a broad range of surface and subsurface habitats, such as marine water, freshwater, freshwater beach sands [4] hydrothermal vents [5], cold-water geyser [6,7], plant rhizosphere [8], alpine permafrost [9], permafrost thaw ponds [10], and many more habitats [11] including the human oral cavity [12][13][14]. Nevertheless, they dominate the groundwater, where they comprise 20-70% of the total microbial community [15][16][17][18] along with thermokarst lakes [19] and hypersaline soda lake sediments [20].…”

Section: Introductionmentioning

confidence: 99%

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The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

Chaudhari

Overholt

Figueroa-Gonzalez

et al. 2021

Preprint

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Aim: The highly diverse Cand. Patescibacteria are predicted to have minimal biosynthetic and metabolic pathways, which hinders understanding of how their populations differentiate to environmental drivers or host organisms. Their metabolic traits to cope with oxidative stress are largely unknown. Here, we utilized genome-resolved metagenomics to investigate the adaptive genome repertoire of Patescibacteria in oxic and anoxic groundwaters, and to infer putative host ranges. Key findings: Within six groundwater wells, Cand. Patescibacteria was the most dominant (up to 79%) super-phylum across 32 metagenomes obtained from sequential 0.2 and 0.1 μm filtration. Of the reconstructed 1275 metagenome-assembled genomes (MAGs), 291 high-quality MAGs were classified as Cand. Patescibacteria. Cand. Paceibacteria and Cand. Microgenomates were enriched exclusively in the 0.1 μm fractions, whereas candidate division ABY1 and Cand. Gracilibacteria were enriched in the 0.2 μm fractions. Patescibacteria enriched in the smaller 0.1 μm filter fractions had 22% smaller genomes, 13.4% lower replication measures, higher fraction of rod-shape determining proteins, and genomic features suggesting type IV pili mediated cell-cell attachments. Near-surface wells harbored Patescibacteria with higher replication rates than anoxic downstream wells characterized by longer water residence time. Except prevalence of superoxide dismutase genes in Patescibacteria MAGs enriched in oxic groundwaters (83%), no major metabolic or phylogenetic differences were observed based on oxygen concentrations. The most abundant Patescibacteria MAG in oxic groundwater encoded a nitrate transporter, nitrite reductase, and F-type ATPase, suggesting an alternative energy conservation mechanism. Patescibacteria consistently co-occurred with one another or with members of phyla Nanoarchaeota, Bacteroidota, Nitrospirota, and Omnitrophota. However, only 8% of MAGs showed highly significant one-to-one association, mostly with Omnitrophota. Genes coding for motility and transport functions in certain Patescibacteria were highly similar to genes from other phyla (Omnitrophota, Proteobacteria, and Nanoarchaeota). Conclusions: Other than genes to cope with oxidative stress, we found little genomic evidence for niche adaptation of Patescibacteria to oxic or anoxic groundwaters. Given that we could detect specific host preference only for a few MAGs, we propose that the majority of Patescibacteria can attach to multiple hosts just long enough to loot or exchange supplies with an economic lifestyle of little preference for geochemical conditions.

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Section: Discussionmentioning

confidence: 49%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

Chaudhari

Overholt

Figueroa-Gonzalez

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…One hundred eighty-eight genomes were obtained from groundwater samples from Genasci Dairy Farm, located in Modesto, CA, United States (He et al, 2021). Over 400 L of groundwater were filtered from monitoring well 5 on Genasci Dairy Farm over a period ranging from March 2017 to June 2018.…”

Section: Genome Collectionmentioning

confidence: 99%

Protein Family Content Uncovers Lineage Relationships and Bacterial Pathway Maintenance Mechanisms in DPANN Archaea

et al. 2021

Self Cite

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DPANN are small-celled archaea that are generally predicted to be symbionts, and in some cases are known episymbionts of other archaea. As the monophyly of the DPANN remains uncertain, we hypothesized that proteome content could reveal relationships among DPANN lineages, constrain genetic overlap with bacteria, and illustrate how organisms with hybrid bacterial and archaeal protein sets might function. We tested this hypothesis using protein family content that was defined in part using 3,197 genomes including 569 newly reconstructed genomes. Protein family content clearly separates the final set of 390 DPANN genomes from other archaea, paralleling the separation of Candidate Phyla Radiation (CPR) bacteria from all other bacteria. This separation is partly driven by hypothetical proteins, some of which may be symbiosis-related. Pacearchaeota with the most limited predicted metabolic capacities have Form II/III and III-like Rubisco, suggesting metabolisms based on scavenged nucleotides. Intriguingly, the Pacearchaeota and Woesearchaeota with the smallest genomes also tend to encode large extracellular murein-like lytic transglycosylase domain proteins that may bind and degrade components of bacterial cell walls, indicating that some might be episymbionts of bacteria. The pathway for biosynthesis of bacterial isoprenoids is widespread in Woesearchaeota genomes and is encoded in proximity to genes involved in bacterial fatty acids synthesis. Surprisingly, in some DPANN genomes we identified a pathway for synthesis of queuosine, an unusual nucleotide in tRNAs of bacteria. Other bacterial systems are predicted to be involved in protein refolding. For example, many DPANN have the complete bacterial DnaK-DnaJ-GrpE system and many Woesearchaeota and Pacearchaeota possess bacterial group I chaperones. Thus, many DPANN appear to have mechanisms to ensure efficient protein folding of both archaeal and laterally acquired bacterial proteins.

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“…Two other large clusters are also prominent: one contains mostly Betaproteobacteria ( Burkholderiales and Neisseriales ), and another contains Bacteroidetes ( Figure 2 ). Finally, a distinct set of Chloroflexi sequences is also observed, including the genes from Litorilinea aerophila (GenBank ID OUC06986.1, unpublished), Caldilinea aerophila [ 104 ], and Aggregatilinea lenta [ 105 ], as well as numerous genes belonging to anaerobic ammonium oxidation (anammox) bacterial community members [ 106 , 107 , 108 , 109 , 110 , 111 , 112 , 113 , 114 , 115 ] such as Candidatus Denitrolinea symbiosum [ 116 ].…”

Section: Natural Diversity Of Nitrate- and Nitrite-sensing Histidine Kinasesmentioning

confidence: 99%

Nitrate- and Nitrite-Sensing Histidine Kinases: Function, Structure, and Natural Diversity

Gushchin

Aleksenko

Orekhov

et al. 2021

IJMS

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Under anaerobic conditions, bacteria may utilize nitrates and nitrites as electron acceptors. Sensitivity to nitrous compounds is achieved via several mechanisms, some of which rely on sensor histidine kinases (HKs). The best studied nitrate- and nitrite-sensing HKs (NSHKs) are NarQ and NarX from Escherichia coli. Here, we review the function of NSHKs, analyze their natural diversity, and describe the available structural information. In particular, we show that around 6000 different NSHK sequences forming several distinct clusters may now be found in genomic databases, comprising mostly the genes from Beta- and Gammaproteobacteria as well as from Bacteroidetes and Chloroflexi, including those from anaerobic ammonia oxidation (annamox) communities. We show that the architecture of NSHKs is mostly conserved, although proteins from Bacteroidetes lack the HAMP and GAF-like domains yet sometimes have PAS. We reconcile the variation of NSHK sequences with atomistic models and pinpoint the structural elements important for signal transduction from the sensor domain to the catalytic module over the transmembrane and cytoplasmic regions spanning more than 200 Å.

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Genome-resolved metagenomics reveals site-specific diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems

Cited by 146 publications

References 88 publications

The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

The economical lifestyle of CPR bacteria in groundwater allows little preference for environmental drivers

Protein Family Content Uncovers Lineage Relationships and Bacterial Pathway Maintenance Mechanisms in DPANN Archaea

Nitrate- and Nitrite-Sensing Histidine Kinases: Function, Structure, and Natural Diversity

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