School of Geography, Earth and Atmospheric Sciences - Research Publications
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ItemPartitioning of Mg, Sr, Ba and U into a subaqueous calcite speleothem(PERGAMON-ELSEVIER SCIENCE LTD, 2019-11-01)The trace-element geochemistry of speleothems is becoming increasingly used for reconstructing palaeoclimate, with a particular emphasis on elements whose concentrations vary according to hydrological conditions at the cave site (e.g. Mg, Sr, Ba and U). An important step in interpreting trace-element abundances is understanding the underlying processes of their incorporation. This includes quantifying the fractionation between the solution and speleothem carbonate via partition coefficients (where the partitioning (D) of element X (DX) is the molar ratio [X/Ca] in the calcite divided by the molar ratio [X/Ca] in the parent water) and evaluating the degree of spatial variability across time-constant speleothem layers. Previous studies of how these elements are incorporated into speleothems have focused primarily on stalagmites and their source waters in natural cave settings, or have used synthetic solutions under cave-analogue laboratory conditions to produce similar dripstones. However, dripstones are not the only speleothem types capable of yielding useful palaeoclimate information. In this study, we investigate the incorporation of Mg, Sr, Ba and U into a subaqueous calcite speleothem (CD3) growing in a natural cave pool in Italy. Pool-water measurements extending back 15 years reveal a remarkably stable geochemical environment owing to the deep cave setting, enabling the calculation of precise solution [X/Ca]. We determine the trace element variability of ‘modern’ subaqueous calcite from a drill core taken through CD3 to derive DMg, DSr, DBa and DU then compare these with published cave, cave-analogue and seawater-analogue studies. The DMg for CD3 is anomalously high (0.042 ± 0.002) compared to previous estimates at similar temperatures (∼8 °C). The DSr (0.100 ± 0.007) is similar to previously reported values, but data from this study as well as those from Tremaine and Froelich (2013) and Day and Henderson (2013) suggest that [Na/Sr] might play an important role in Sr incorporation through the potential for Na to outcompete Sr for calcite non-lattice sites. DBa in CD3 (0.086 ± 0.008) is similar to values derived by Day and Henderson (2013) under cave-analogue conditions, whilst DU (0.013 ± 0.002) is almost an order of magnitude lower, possibly due to the unusually slow speleothem growth rates (<1 μm a−1), which could expose the crystal surfaces to leaching of uranyl carbonate. Finally, laser-ablation ICP-MS analysis of the upper 7 μm of CD3, regarded as ‘modern’ for the purposes of this study, reveals considerable heterogeneity, particularly for Sr, Ba and U, which is potentially indicative of compositional zoning. This reinforces the need to conduct 2D mapping and/or multiple laser passes to capture the range of time-equivalent elemental variations prior to palaeoclimate interpretation.
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ItemGenome-resolved metagenomics of eukaryotic populations during early colonization of premature infants and in hospital rooms.(Springer Science and Business Media LLC, 2019-02-15)BACKGROUND: Fungal infections are a significant cause of mortality and morbidity in hospitalized preterm infants, yet little is known about eukaryotic colonization of infants and of the neonatal intensive care unit as a possible source of colonizing strains. This is partly because microbiome studies often utilize bacterial 16S rRNA marker gene sequencing, a technique that is blind to eukaryotic organisms. Knowledge gaps exist regarding the phylogeny and microdiversity of eukaryotes that colonize hospitalized infants, as well as potential reservoirs of eukaryotes in the hospital room built environment. RESULTS: Genome-resolved analysis of 1174 time-series fecal metagenomes from 161 premature infants revealed fungal colonization of 10 infants. Relative abundance levels reached as high as 97% and were significantly higher in the first weeks of life (p = 0.004). When fungal colonization occurred, multiple species were present more often than expected by random chance (p = 0.008). Twenty-four metagenomic samples were analyzed from hospital rooms of six different infants. Compared to floor and surface samples, hospital sinks hosted diverse and highly variable communities containing genomically novel species, including from Diptera (fly) and Rhabditida (worm) for which genomes were assembled. With the exception of Diptera and two other organisms, zygosity of the newly assembled diploid eukaryote genomes was low. Interestingly, Malassezia and Candida species were present in both room and infant gut samples. CONCLUSIONS: Increased levels of fungal co-colonization may reflect synergistic interactions or differences in infant susceptibility to fungal colonization. Discovery of eukaryotic organisms that have not been sequenced previously highlights the benefit of genome-resolved analyses, and low zygosity of assembled genomes could reflect inbreeding or strong selection imposed by room conditions.
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ItemLateral Gene Transfer Shapes the Distribution of RuBisCO among Candidate Phyla Radiation Bacteria and DPANN Archaea.(Oxford University Press (OUP), 2019-03-01)Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is considered to be the most abundant enzyme on Earth. Despite this, its full diversity and distribution across the domains of life remain to be determined. Here, we leverage a large set of bacterial, archaeal, and viral genomes recovered from the environment to expand our understanding of existing RuBisCO diversity and the evolutionary processes responsible for its distribution. Specifically, we report a new type of RuBisCO present in Candidate Phyla Radiation (CPR) bacteria that is related to the archaeal Form III enzyme and contains the amino acid residues necessary for carboxylase activity. Genome-level metabolic analyses supported the inference that these RuBisCO function in a CO2-incorporating pathway that consumes nucleotides. Importantly, some Gottesmanbacteria (CPR) also encode a phosphoribulokinase that may augment carbon metabolism through a partial Calvin-Benson-Bassham cycle. Based on the scattered distribution of RuBisCO and its discordant evolutionary history, we conclude that this enzyme has been extensively laterally transferred across the CPR bacteria and DPANN archaea. We also report RuBisCO-like proteins in phage genomes from diverse environments. These sequences cluster with proteins in the Beckwithbacteria (CPR), implicating phage as a possible mechanism of RuBisCO transfer. Finally, we synthesize our metabolic and evolutionary analyses to suggest that lateral gene transfer of RuBisCO may have facilitated major shifts in carbon metabolism in several important bacterial and archaeal lineages.
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ItemMetagenomic recovery of two distinct comammox Nitrospira from the terrestrial subsurface.(Wiley, 2019-10)The recently discovered comammox process encompasses both nitrification steps, the aerobic oxidation of ammonia and nitrite, in a single organism. All known comammox bacteria are affiliated with Nitrospira sublineage II and can be grouped into two distinct clades, referred to as A and B, based on ammonia monooxygenase phylogeny. In this study, we report high-quality draft genomes of two novel comammox Nitrospira from the terrestrial subsurface, representing one clade A and one clade B comammox organism. The two metagenome-assembled genomes were compared with other representatives of Nitrospira sublineage II, including both canonical and comammox Nitrospira. Phylogenomic analyses confirmed the affiliation of the two novel Nitrospira with comammox clades A and B respectively. Based on phylogenetic distance and pairwise average nucleotide identity values, both comammox Nitrospira were classified as novel species. Genomic comparison revealed high conservation of key metabolic features in sublineage II Nitrospira, including respiratory complexes I-V and the machineries for nitrite oxidation and carbon fixation via the reductive tricarboxylic acid cycle. In addition, the presence of the enzymatic repertoire for formate and hydrogen oxidation in the Rifle clades A and B comammox genomes, respectively, suggest a broader distribution of these metabolic features than previously anticipated.
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ItemCandidate Phyla Radiation Roizmanbacteria From Hot Springs Have Novel and Unexpectedly Abundant CRISPR-Cas Systems.(Frontiers Media SA, 2019)The Candidate Phyla Radiation (CPR) comprises a huge group of bacteria that have small genomes that rarely encode CRISPR-Cas systems for phage defense. Consequently, questions remain about their mechanisms of phage resistance and the nature of phage that infect them. The compact CRISPR-CasY system (Cas12d) with potential value in genome editing was first discovered in these organisms. Relatively few CasY sequences have been reported to date, and little is known about the function and activity of these systems in the natural environment. Here, we conducted a genome-resolved metagenomic investigation of hot spring microbiomes and recovered CRISPR systems mostly from Roizmanbacteria that involve CasY proteins that are divergent from published sequences. Within population diversity in the spacer set indicates current in situ diversification of most of the loci. In addition to CasY, some Roizmanbacteria genomes also encode large type I-B and/or III-A systems that, based on spacer targeting, are used in phage defense. CRISPR targeting identified three phage represented by complete genomes and a prophage, which are the first reported for bacteria of the Microgenomates superphylum. Interestingly, one phage encodes a Cas4-like protein, a scenario that has been suggested to drive acquisition of self-targeting spacers. Consistent with this, the Roizmanbacteria population that it infects has a CRISPR locus that includes self-targeting spacers and a fragmented CasY gene (fCasY). Despite gene fragmentation, the PAM sequence is the same as that of other CasY reported in this study. Fragmentation of CasY may avoid the lethality of self-targeting spacers. However, the spacers may still have some biological role, possibly in genome regulation. The findings expand our understanding of CasY diversity, and more broadly, CRISPR-Cas systems and phage of CPR bacteria.
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ItemPutative Mixotrophic Nitrifying-Denitrifying Gammaproteobacteria Implicated in Nitrogen Cycling Within the Ammonia/Oxygen Transition Zone of an Oil Sands Pit Lake.(Frontiers Media SA, 2019)Anthropogenically-impacted environments offer the opportunity to discover novel microbial species and metabolisms, which may be undetectable in natural systems. Here, a combined metagenomic and geochemical study in Base Mine Lake, Alberta, Canada, which is the only oil sands end pit lake to date, revealed that nitrification was performed by members from Nitrosomonadaceae, Chloroflexi and unclassified Gammaproteobacteria "MBAE14." While Nitrosomonadaceae and Chloroflexi groups were relatively abundant in the upper oxygenated zones, MBAE14 dominated the hypoxic hypolimnetic zones (approximately 30% of total microbial communities); MBAE14 was not detected in the underlying anoxic tailings. Replication rate analyses indicate that MBAE14 grew in metalimnetic and hypolimnetic water cap regions, most actively at the metalimnetic, ammonia/oxygen transition zone consistent with it putatively conducting nitrification. Detailed genomic analyses of MBAE14 evidenced both ammonia oxidation and denitrification into dinitrogen capabilities. However, the absence of known CO2-fixation genes suggests a heterotrophic denitrifying metabolism. Functional marker genes of ammonia oxidation (amo and hao) in the MBAE14 genome are homologous with those conserved in autotrophic nitrifiers, but not with those of known heterotrophic nitrifiers. We propose that this novel MBAE14 inhabits the specific ammonia-rich, oxygen and labile organic matter-limited conditions occurring in Base Mine Lake which selectively favors mixotrophic coupled nitrifier denitrification metabolism. Our results highlight the opportunities to better constrain biogeochemical cycles from the application of metagenomics to engineered systems associated with extractive resource sectors.
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ItemMetatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil.(Proceedings of the National Academy of Sciences, 2019-12-17)Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health, and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in soil, 1 of the most complex microbial systems. Here, we assembled 48 individual metatranscriptomes from 4 habitats within a planted soil sampled over a 22-d time series: Rhizosphere alone, detritosphere alone, rhizosphere with added root detritus, and unamended soil (4 time points and 3 biological replicates). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker genes. Based on viral phylogeny, much of the diversity was Narnaviridae that may parasitize fungi or Leviviridae, which may infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral and host communities were structured based on the presence of root litter. Clear temporal dynamics by Leviviridae and their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant, and active in soil. When viral infection causes host cell death, it may mobilize cell carbon in a process that may represent an overlooked component of soil carbon cycling.
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ItemUnusual Metabolism and Hypervariation in the Genome of a Gracilibacterium (BD1-5) from an Oil-Degrading Community.(American Society for Microbiology, 2019-11-12)The candidate phyla radiation (CPR) comprises a large monophyletic group of bacterial lineages known almost exclusively based on genomes obtained using cultivation-independent methods. Within the CPR, Gracilibacteria (BD1-5) are particularly poorly understood due to undersampling and the inherent fragmented nature of available genomes. Here, we report the first closed, curated genome of a gracilibacterium from an enrichment experiment inoculated from the Gulf of Mexico and designed to investigate hydrocarbon degradation. The gracilibacterium rose in abundance after the community switched to dominance by Colwellia Notably, we predict that this gracilibacterium completely lacks glycolysis, the pentose phosphate and Entner-Doudoroff pathways. It appears to acquire pyruvate, acetyl coenzyme A (acetyl-CoA), and oxaloacetate via degradation of externally derived citrate, malate, and amino acids and may use compound interconversion and oxidoreductases to generate and recycle reductive power. The initial genome assembly was fragmented in an unusual gene that is hypervariable within a repeat region. Such extreme local variation is rare but characteristic of genes that confer traits under pressure to diversify within a population. Notably, the four major repeated 9-mer nucleotide sequences all generate a proline-threonine-aspartic acid (PTD) repeat. The genome of an abundant Colwellia psychrerythraea population has a large extracellular protein that also contains the repeated PTD motif. Although we do not know the host for the BD1-5 cell, the high relative abundance of the C. psychrerythraea population and the shared surface protein repeat may indicate an association between these bacteria.IMPORTANCE CPR bacteria are generally predicted to be symbionts due to their extensive biosynthetic deficits. Although monophyletic, they are not monolithic in terms of their lifestyles. The organism described here appears to have evolved an unusual metabolic platform not reliant on glucose or pentose sugars. Its biology appears to be centered around bacterial host-derived compounds and/or cell detritus. Amino acids likely provide building blocks for nucleic acids, peptidoglycan, and protein synthesis. We resolved an unusual repeat region that would be invisible without genome curation. The nucleotide sequence is apparently under strong diversifying selection, but the amino acid sequence is under stabilizing selection. The amino acid repeat also occurs in a surface protein of a coexisting bacterium, suggesting colocation and possibly interdependence.
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ItemGenome-Resolved Proteomic Stable Isotope Probing of Soil Microbial Communities Using 13CO2 and 13C-Methanol.(Frontiers Media SA, 2019)Stable isotope probing (SIP) enables tracking the nutrient flows from isotopically labeled substrates to specific microorganisms in microbial communities. In proteomic SIP, labeled proteins synthesized by the microbial consumers of labeled substrates are identified with a shotgun proteomics approach. Here, proteomic SIP was combined with targeted metagenomic binning to reconstruct metagenome-assembled genomes (MAGs) of the microorganisms producing labeled proteins. This approach was used to track carbon flows from 13CO2 to the rhizosphere communities of Zea mays, Triticum aestivum, and Arabidopsis thaliana. Rhizosphere microorganisms that assimilated plant-derived 13C were capable of metabolic and signaling interactions with their plant hosts, as shown by their MAGs containing genes for phytohormone modulation, quorum sensing, and transport and metabolism of nutrients typical of those found in root exudates. XoxF-type methanol dehydrogenases were among the most abundant proteins identified in the rhizosphere metaproteomes. 13C-methanol proteomic SIP was used to test the hypothesis that XoxF was used to metabolize and assimilate methanol in the rhizosphere. We detected 7 13C-labeled XoxF proteins and identified methylotrophic pathways in the MAGs of 8 13C-labeled microorganisms, which supported the hypothesis. These two studies demonstrated the capability of proteomic SIP for functional characterization of active microorganisms in complex microbial communities.
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ItemImpacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network.(Oxford University Press (OUP), 2019-06)Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found in sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.
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