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Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics.

Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, Dupont CL, Casamayor EO - ISME J (2015)

Bottom Line: Bacteroidales were also abundant and showed potential for dissimilatory nitrate reduction to ammonium.We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments.Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.

View Article: PubMed Central - PubMed

Affiliation: Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes-Spanish Council for Research (CEAB-CSIC), Blanes, Girona, Spain.

ABSTRACT
Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and in silico reconstruction of carbon, nitrogen and sulfur metabolic pathways that were tightly coupled through a few bacterial groups. The potential for nitrogen fixation and denitrification was detected in both autotrophs and heterotrophs, with a major role for nitrogen and carbon fixations in Chlorobiaceae. Campylobacterales accounted for a large percentage of denitrification genes, while Gallionellales were putatively involved in denitrification, iron oxidation and carbon fixation and may have a major role in the biogeochemistry of the iron cycle. Bacteroidales were also abundant and showed potential for dissimilatory nitrate reduction to ammonium. The very low abundance of genes for nitrification, the minor presence of anammox genes, the high potential for nitrogen fixation and mineralization and the potential for chemotrophic CO2 fixation and CO oxidation all provide potential clues on the anoxic zones functioning. We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments. Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.

No MeSH data available.


Related in: MedlinePlus

Genetic potential for several steps of the nitrogen cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the nitrogen pathways (100% value, see Supplementary Table S3). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **Presence of AOA, AOB and nitrite-oxidizing bacteria (NOB) reads in the metagenomic pool.
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fig5: Genetic potential for several steps of the nitrogen cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the nitrogen pathways (100% value, see Supplementary Table S3). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **Presence of AOA, AOB and nitrite-oxidizing bacteria (NOB) reads in the metagenomic pool.

Mentions: As Bacteria and Archaea accounted for most of total metagenomic reads, we focused on the prokaryotes for a comparative study of the geochemistry of carbon (Figure 4), nitrogen (Figure 5) and sulfur (Figure 6) along the redoxcline. We used the relative abundance of the detected functional genes as a proxy of the potential relevance of each pathway in situ without considering the role of microscopic algae. For the C cycling, the main pathway detected in the oxic–anoxic interface was aerobic respiration by heterotrophic Actinomycetales and Burkholderiales in Lake Cisó, and by Actinomycetales and Pelagibacterales (SAR11-like) in Lake Banyoles C-III. In the hypolimnion, the abundant pathways were various forms of anaerobic carbon fixation: by Chromatiales (anoxygenic phototrophy by the Calvin cycle), Bacteroidales (probably anaplerotic) and sulfate-reducing bacteria (SRB) (probably the reductive citric acid cycle/Arnon pathway; Fuchs, 2011) in Lake Cisó, and Chlorobiales (anoxygenic phototrophy by the Arnon cycle) in Banyoles C-III (Table 3). Chemolithotrophic aerobic carbon fixation via the Calvin cycle, which was rare, was mostly related to Betaproteobacteria of the genus Hydrogenophilales (Thiobacillus-like) and Gallionellales (Syderoxydans-like). Chemolithotrophic Epsilonproteobacteria with genes for the Arnon cycle (Campylobacterales on Figure 4) were found related to the genera Arcobacter, Sulfuricurvum and Sulfurimonas (Table 3). Carbon monoxide (CO) oxidation marker genes were also present (3–14% of those targeted marker genes selected for the carbon cycle, Supplementary Table S3) and related to heterotrophic bacteria. The potential for fermentation was mostly observed in Lake Cisó. Both methanogenesis and methane oxidation-specific marker genes had low abundances in all four environments, and even in those samples where such genes were not specifically detected (Figure 4, dotted lines) we found additional metagenomic reads taxonomically matching methanogens and methane oxidizers clades.


Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics.

Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, Dupont CL, Casamayor EO - ISME J (2015)

Genetic potential for several steps of the nitrogen cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the nitrogen pathways (100% value, see Supplementary Table S3). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **Presence of AOA, AOB and nitrite-oxidizing bacteria (NOB) reads in the metagenomic pool.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4478705&req=5

fig5: Genetic potential for several steps of the nitrogen cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the nitrogen pathways (100% value, see Supplementary Table S3). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **Presence of AOA, AOB and nitrite-oxidizing bacteria (NOB) reads in the metagenomic pool.
Mentions: As Bacteria and Archaea accounted for most of total metagenomic reads, we focused on the prokaryotes for a comparative study of the geochemistry of carbon (Figure 4), nitrogen (Figure 5) and sulfur (Figure 6) along the redoxcline. We used the relative abundance of the detected functional genes as a proxy of the potential relevance of each pathway in situ without considering the role of microscopic algae. For the C cycling, the main pathway detected in the oxic–anoxic interface was aerobic respiration by heterotrophic Actinomycetales and Burkholderiales in Lake Cisó, and by Actinomycetales and Pelagibacterales (SAR11-like) in Lake Banyoles C-III. In the hypolimnion, the abundant pathways were various forms of anaerobic carbon fixation: by Chromatiales (anoxygenic phototrophy by the Calvin cycle), Bacteroidales (probably anaplerotic) and sulfate-reducing bacteria (SRB) (probably the reductive citric acid cycle/Arnon pathway; Fuchs, 2011) in Lake Cisó, and Chlorobiales (anoxygenic phototrophy by the Arnon cycle) in Banyoles C-III (Table 3). Chemolithotrophic aerobic carbon fixation via the Calvin cycle, which was rare, was mostly related to Betaproteobacteria of the genus Hydrogenophilales (Thiobacillus-like) and Gallionellales (Syderoxydans-like). Chemolithotrophic Epsilonproteobacteria with genes for the Arnon cycle (Campylobacterales on Figure 4) were found related to the genera Arcobacter, Sulfuricurvum and Sulfurimonas (Table 3). Carbon monoxide (CO) oxidation marker genes were also present (3–14% of those targeted marker genes selected for the carbon cycle, Supplementary Table S3) and related to heterotrophic bacteria. The potential for fermentation was mostly observed in Lake Cisó. Both methanogenesis and methane oxidation-specific marker genes had low abundances in all four environments, and even in those samples where such genes were not specifically detected (Figure 4, dotted lines) we found additional metagenomic reads taxonomically matching methanogens and methane oxidizers clades.

Bottom Line: Bacteroidales were also abundant and showed potential for dissimilatory nitrate reduction to ammonium.We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments.Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.

View Article: PubMed Central - PubMed

Affiliation: Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes-Spanish Council for Research (CEAB-CSIC), Blanes, Girona, Spain.

ABSTRACT
Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and in silico reconstruction of carbon, nitrogen and sulfur metabolic pathways that were tightly coupled through a few bacterial groups. The potential for nitrogen fixation and denitrification was detected in both autotrophs and heterotrophs, with a major role for nitrogen and carbon fixations in Chlorobiaceae. Campylobacterales accounted for a large percentage of denitrification genes, while Gallionellales were putatively involved in denitrification, iron oxidation and carbon fixation and may have a major role in the biogeochemistry of the iron cycle. Bacteroidales were also abundant and showed potential for dissimilatory nitrate reduction to ammonium. The very low abundance of genes for nitrification, the minor presence of anammox genes, the high potential for nitrogen fixation and mineralization and the potential for chemotrophic CO2 fixation and CO oxidation all provide potential clues on the anoxic zones functioning. We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments. Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.

No MeSH data available.


Related in: MedlinePlus