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Metagenomic evidence for metabolism of trace atmospheric gases by high-elevation desert Actinobacteria.

Lynch RC, Darcy JL, Kane NC, Nemergut DR, Schmidt SK - Front Microbiol (2014)

Bottom Line: The phylogenetic structure of this community is significantly under dispersed, with actinobacterial lineages making up 97.9-98.6% of the 16S rRNA genes, suggesting a high degree of environmental selection.We compared genomic content among related Pseudonocardia spp. and estimated rates of non-synonymous and synonymous nucleic acid substitutions between protein coding homologs.Collectively, these comparative analyses suggest that the community structure and various functional genes have undergone strong selection in the nutrient poor desert mineral soils and high-elevation atmospheric conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado Boulder, CO, USA.

ABSTRACT
Previous surveys of very dry Atacama Desert mineral soils have consistently revealed sparse communities of non-photosynthetic microbes. The functional nature of these microorganisms remains debatable given the harshness of the environment and low levels of biomass and diversity. The aim of this study was to gain an understanding of the phylogenetic community structure and metabolic potential of a low-diversity mineral soil metagenome that was collected from a high-elevation Atacama Desert volcano debris field. We pooled DNA extractions from over 15 g of volcanic material, and using whole genome shotgun sequencing, observed only 75-78 total 16S rRNA gene OTUs3%. The phylogenetic structure of this community is significantly under dispersed, with actinobacterial lineages making up 97.9-98.6% of the 16S rRNA genes, suggesting a high degree of environmental selection. Due to this low diversity and uneven community composition, we assembled and analyzed the metabolic pathways of the most abundant genome, a Pseudonocardia sp. (56-72% of total 16S genes). Our assembly and binning efforts yielded almost 4.9 Mb of Pseudonocardia sp. contigs, which accounts for an estimated 99.3% of its non-repetitive genomic content. This genome contains a limited array of carbohydrate catabolic pathways, but encodes for CO2 fixation via the Calvin cycle. The genome also encodes complete pathways for the catabolism of various trace gases (H2, CO and several organic C1 compounds) and the assimilation of ammonia and nitrate. We compared genomic content among related Pseudonocardia spp. and estimated rates of non-synonymous and synonymous nucleic acid substitutions between protein coding homologs. Collectively, these comparative analyses suggest that the community structure and various functional genes have undergone strong selection in the nutrient poor desert mineral soils and high-elevation atmospheric conditions.

No MeSH data available.


Related in: MedlinePlus

Inventories of gene functional categories, comparing non-desert (gray), desert (black) biomes to the high-elevation volcano metagenomes (blue). Asterisks indicate Bonferroni corrected significant differences (P < 0.0009) between the volcano data and desert or non-desert data (desert to non-desert comparisons not shown) for all pairwise T-tests.
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Figure 2: Inventories of gene functional categories, comparing non-desert (gray), desert (black) biomes to the high-elevation volcano metagenomes (blue). Asterisks indicate Bonferroni corrected significant differences (P < 0.0009) between the volcano data and desert or non-desert data (desert to non-desert comparisons not shown) for all pairwise T-tests.

Mentions: The Llullaillaco metagenomes show a pronounced reduction in genes associated with carbohydrate metabolism compared with other desert and non-desert metagenomes (Figure 2). By contrast we found significant enrichment of pathways categorized as membrane transport, nucleotide metabolism, regulation and cell signaling, nitrogen metabolism and virulence and defense. Examining the presence and absence of metabolic pathways within the total metagenome, we found no evidence for complete photosynthetic pathways, yet found complete gene sets for the oxidation of CO and H2, and for CO2 fixation with the Calvin cycle. Methylotrophic pathways also suggest a role for other C1 compound oxidation and assimilation including: methanol, formaldehyde, formate and perhaps methane. No nitrogen (N2) fixation or ammonia monooxygenase genes were identified, but genes for nitrate (NO−3) reduction (nitrate reductase) and ammonia (NH3) assimilation (glutamine synthetase) were found in high abundance.


Metagenomic evidence for metabolism of trace atmospheric gases by high-elevation desert Actinobacteria.

Lynch RC, Darcy JL, Kane NC, Nemergut DR, Schmidt SK - Front Microbiol (2014)

Inventories of gene functional categories, comparing non-desert (gray), desert (black) biomes to the high-elevation volcano metagenomes (blue). Asterisks indicate Bonferroni corrected significant differences (P < 0.0009) between the volcano data and desert or non-desert data (desert to non-desert comparisons not shown) for all pairwise T-tests.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4269115&req=5

Figure 2: Inventories of gene functional categories, comparing non-desert (gray), desert (black) biomes to the high-elevation volcano metagenomes (blue). Asterisks indicate Bonferroni corrected significant differences (P < 0.0009) between the volcano data and desert or non-desert data (desert to non-desert comparisons not shown) for all pairwise T-tests.
Mentions: The Llullaillaco metagenomes show a pronounced reduction in genes associated with carbohydrate metabolism compared with other desert and non-desert metagenomes (Figure 2). By contrast we found significant enrichment of pathways categorized as membrane transport, nucleotide metabolism, regulation and cell signaling, nitrogen metabolism and virulence and defense. Examining the presence and absence of metabolic pathways within the total metagenome, we found no evidence for complete photosynthetic pathways, yet found complete gene sets for the oxidation of CO and H2, and for CO2 fixation with the Calvin cycle. Methylotrophic pathways also suggest a role for other C1 compound oxidation and assimilation including: methanol, formaldehyde, formate and perhaps methane. No nitrogen (N2) fixation or ammonia monooxygenase genes were identified, but genes for nitrate (NO−3) reduction (nitrate reductase) and ammonia (NH3) assimilation (glutamine synthetase) were found in high abundance.

Bottom Line: The phylogenetic structure of this community is significantly under dispersed, with actinobacterial lineages making up 97.9-98.6% of the 16S rRNA genes, suggesting a high degree of environmental selection.We compared genomic content among related Pseudonocardia spp. and estimated rates of non-synonymous and synonymous nucleic acid substitutions between protein coding homologs.Collectively, these comparative analyses suggest that the community structure and various functional genes have undergone strong selection in the nutrient poor desert mineral soils and high-elevation atmospheric conditions.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, University of Colorado Boulder, CO, USA.

ABSTRACT
Previous surveys of very dry Atacama Desert mineral soils have consistently revealed sparse communities of non-photosynthetic microbes. The functional nature of these microorganisms remains debatable given the harshness of the environment and low levels of biomass and diversity. The aim of this study was to gain an understanding of the phylogenetic community structure and metabolic potential of a low-diversity mineral soil metagenome that was collected from a high-elevation Atacama Desert volcano debris field. We pooled DNA extractions from over 15 g of volcanic material, and using whole genome shotgun sequencing, observed only 75-78 total 16S rRNA gene OTUs3%. The phylogenetic structure of this community is significantly under dispersed, with actinobacterial lineages making up 97.9-98.6% of the 16S rRNA genes, suggesting a high degree of environmental selection. Due to this low diversity and uneven community composition, we assembled and analyzed the metabolic pathways of the most abundant genome, a Pseudonocardia sp. (56-72% of total 16S genes). Our assembly and binning efforts yielded almost 4.9 Mb of Pseudonocardia sp. contigs, which accounts for an estimated 99.3% of its non-repetitive genomic content. This genome contains a limited array of carbohydrate catabolic pathways, but encodes for CO2 fixation via the Calvin cycle. The genome also encodes complete pathways for the catabolism of various trace gases (H2, CO and several organic C1 compounds) and the assimilation of ammonia and nitrate. We compared genomic content among related Pseudonocardia spp. and estimated rates of non-synonymous and synonymous nucleic acid substitutions between protein coding homologs. Collectively, these comparative analyses suggest that the community structure and various functional genes have undergone strong selection in the nutrient poor desert mineral soils and high-elevation atmospheric conditions.

No MeSH data available.


Related in: MedlinePlus