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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

Ecophysiological overview of the volcano Pseudonocardia sp. metabolic pathways as inferred from assembled metagenomic data. sMMO, soluble methane monooxygenase; MDH, (PQQ)-dependent methanol dehydrogenase; FDH, formaldehyde dehydrogenase; FoDH formate dehydrogenase-O; NDH, group 5 high-affinity NiFe hydrogenase, ATPS, ATP synthase; ETC electron transport chain; COD, form I carbon monoxide dehydrogenase; AsE, arsenite efflux; CYP, cyanate permease; CYL cyanate lyase; AMI, ammonium importer; NAS, assimilatory nitrate reductase; NAR, respiratory nitrate reductase; NIE, nitrite extrusion protein; NIR, nitrite reductase; GS, glutamine synthetase; SPM, sulfate permease; 3PG 3-phosphoglyceric acid; PHB, polyhydroxybutyrate; Gln, glutamine.
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Figure 5: Ecophysiological overview of the volcano Pseudonocardia sp. metabolic pathways as inferred from assembled metagenomic data. sMMO, soluble methane monooxygenase; MDH, (PQQ)-dependent methanol dehydrogenase; FDH, formaldehyde dehydrogenase; FoDH formate dehydrogenase-O; NDH, group 5 high-affinity NiFe hydrogenase, ATPS, ATP synthase; ETC electron transport chain; COD, form I carbon monoxide dehydrogenase; AsE, arsenite efflux; CYP, cyanate permease; CYL cyanate lyase; AMI, ammonium importer; NAS, assimilatory nitrate reductase; NAR, respiratory nitrate reductase; NIE, nitrite extrusion protein; NIR, nitrite reductase; GS, glutamine synthetase; SPM, sulfate permease; 3PG 3-phosphoglyceric acid; PHB, polyhydroxybutyrate; Gln, glutamine.

Mentions: The volcano Pseudonocardia sp. genome is at least 4.9 Mb (Table 2) and contains many of the pathways that define the total community metabolic potential (e.g., aerobic heterotrophic metabolism, NO−3 and NH3 utilization, H2 and CO oxidation, CO2 fixation and methylotrophic pathways, Figure 5). Many genes (33%) were found with multiple copies in the genome, suggesting a possible role for gene duplication events during the divergence of this genome. Potential carbohydrate oxidation pathways are quite limited, with genes present only for the utilization of glucose, mannose, ribose, gluconate, maltose, trehalose, lactose, and galactose that feed into the Embden-Meyerhof-Parnas pathway or the pentose phosphate pathway. Carbohydrate uptake potential is apparently even more restricted as only a single annotated maltose ABC importer was identified. A complete list of putative gene annotations can be found in the IMG/ER database (id 45716).


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)

Ecophysiological overview of the volcano Pseudonocardia sp. metabolic pathways as inferred from assembled metagenomic data. sMMO, soluble methane monooxygenase; MDH, (PQQ)-dependent methanol dehydrogenase; FDH, formaldehyde dehydrogenase; FoDH formate dehydrogenase-O; NDH, group 5 high-affinity NiFe hydrogenase, ATPS, ATP synthase; ETC electron transport chain; COD, form I carbon monoxide dehydrogenase; AsE, arsenite efflux; CYP, cyanate permease; CYL cyanate lyase; AMI, ammonium importer; NAS, assimilatory nitrate reductase; NAR, respiratory nitrate reductase; NIE, nitrite extrusion protein; NIR, nitrite reductase; GS, glutamine synthetase; SPM, sulfate permease; 3PG 3-phosphoglyceric acid; PHB, polyhydroxybutyrate; Gln, glutamine.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Ecophysiological overview of the volcano Pseudonocardia sp. metabolic pathways as inferred from assembled metagenomic data. sMMO, soluble methane monooxygenase; MDH, (PQQ)-dependent methanol dehydrogenase; FDH, formaldehyde dehydrogenase; FoDH formate dehydrogenase-O; NDH, group 5 high-affinity NiFe hydrogenase, ATPS, ATP synthase; ETC electron transport chain; COD, form I carbon monoxide dehydrogenase; AsE, arsenite efflux; CYP, cyanate permease; CYL cyanate lyase; AMI, ammonium importer; NAS, assimilatory nitrate reductase; NAR, respiratory nitrate reductase; NIE, nitrite extrusion protein; NIR, nitrite reductase; GS, glutamine synthetase; SPM, sulfate permease; 3PG 3-phosphoglyceric acid; PHB, polyhydroxybutyrate; Gln, glutamine.
Mentions: The volcano Pseudonocardia sp. genome is at least 4.9 Mb (Table 2) and contains many of the pathways that define the total community metabolic potential (e.g., aerobic heterotrophic metabolism, NO−3 and NH3 utilization, H2 and CO oxidation, CO2 fixation and methylotrophic pathways, Figure 5). Many genes (33%) were found with multiple copies in the genome, suggesting a possible role for gene duplication events during the divergence of this genome. Potential carbohydrate oxidation pathways are quite limited, with genes present only for the utilization of glucose, mannose, ribose, gluconate, maltose, trehalose, lactose, and galactose that feed into the Embden-Meyerhof-Parnas pathway or the pentose phosphate pathway. Carbohydrate uptake potential is apparently even more restricted as only a single annotated maltose ABC importer was identified. A complete list of putative gene annotations can be found in the IMG/ER database (id 45716).

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