Diurnal Changes in Active Carbon and Nitrogen Pathways Along the Temperature Gradient in Porcelana Hot Spring Microbial Mat

Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H CO ) and nitrogen ( NH Cl and K NO ) assimilation rates....

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Published in:Frontiers in microbiology Vol. 9; p. 2353
Main Authors: Alcamán-Arias, María E., Pedrós-Alió, Carlos, Tamames, Javier, Fernández, Camila, Pérez-Pantoja, Danilo, Vásquez, Mónica, Díez, Beatriz
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Language:English
Published: Switzerland Frontiers Media 02.10.2018
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Abstract Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H CO ) and nitrogen ( NH Cl and K NO ) assimilation rates. The microbial mat community included 31 phyla, of which only and were dominant. At 58°C both phyla co-occurred, with similar contributions in relative abundances in metagenomes and total transcriptional activity. At 66°C, filamentous anoxygenic phototrophic were >90% responsible for the total transcriptional activity recovered, while contributed most metagenomics and metatranscriptomics reads at 48°C. According to such reads, phototrophy was carried out both through oxygenic photosynthesis by (mostly ) and anoxygenic phototrophy due mainly to . Inorganic carbon assimilation through the Calvin-Benson cycle was almost exclusively due to , which was the main primary producer at lower temperatures. Two other CO fixation pathways were active at certain times and temperatures as indicated by transcripts: 3-hydroxypropionate (3-HP) bi-cycle due to and 3-hydroxypropionate-4-hydroxybutyrate (HH) cycle carried out by . The active transcription of the genes involved in these C-fixation pathways correlated with high determined carbon fixation rates. measurements of ammonia assimilation and nitrogen fixation (exclusively attributed to and mostly to sp.) showed these were the most important nitrogen acquisition pathways at 58 and 48°C. At 66°C ammonia oxidation genes were actively transcribed (mostly due to ). Reads indicated that denitrification was present as a nitrogen sink at all temperatures and that dissimilatory nitrate reduction to ammonia (DNRA) contributed very little. The combination of metagenomic and metatranscriptomic analysis with assimilation rates, allowed the reconstruction of day and night carbon and nitrogen assimilation pathways together with the contribution of keystone microorganisms in this natural hot spring microbial mat.
AbstractList Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H13CO3) and nitrogen (15NH4Cl and K15NO3) assimilation rates. The microbial mat community included 31 phyla, of which only Cyanobacteria and Chloroflexi were dominant. At 58°C both phyla co-occurred, with similar contributions in relative abundances in metagenomes and total transcriptional activity. At 66°C, filamentous anoxygenic phototrophic Chloroflexi were >90% responsible for the total transcriptional activity recovered, while Cyanobacteria contributed most metagenomics and metatranscriptomics reads at 48°C. According to such reads, phototrophy was carried out both through oxygenic photosynthesis by Cyanobacteria (mostly Mastigocladus) and anoxygenic phototrophy due mainly to Chloroflexi. Inorganic carbon assimilation through the Calvin–Benson cycle was almost exclusively due to Mastigocladus, which was the main primary producer at lower temperatures. Two other CO2 fixation pathways were active at certain times and temperatures as indicated by transcripts: 3-hydroxypropionate (3-HP) bi-cycle due to Chloroflexi and 3-hydroxypropionate-4-hydroxybutyrate (HH) cycle carried out by Thaumarchaeota. The active transcription of the genes involved in these C-fixation pathways correlated with high in situ determined carbon fixation rates. In situ measurements of ammonia assimilation and nitrogen fixation (exclusively attributed to Cyanobacteria and mostly to Mastigocladus sp.) showed these were the most important nitrogen acquisition pathways at 58 and 48°C. At 66°C ammonia oxidation genes were actively transcribed (mostly due to Thaumarchaeota). Reads indicated that denitrification was present as a nitrogen sink at all temperatures and that dissimilatory nitrate reduction to ammonia (DNRA) contributed very little. The combination of metagenomic and metatranscriptomic analysis with in situ assimilation rates, allowed the reconstruction of day and night carbon and nitrogen assimilation pathways together with the contribution of keystone microorganisms in this natural hot spring microbial mat.
Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H CO ) and nitrogen ( NH Cl and K NO ) assimilation rates. The microbial mat community included 31 phyla, of which only and were dominant. At 58°C both phyla co-occurred, with similar contributions in relative abundances in metagenomes and total transcriptional activity. At 66°C, filamentous anoxygenic phototrophic were >90% responsible for the total transcriptional activity recovered, while contributed most metagenomics and metatranscriptomics reads at 48°C. According to such reads, phototrophy was carried out both through oxygenic photosynthesis by (mostly ) and anoxygenic phototrophy due mainly to . Inorganic carbon assimilation through the Calvin-Benson cycle was almost exclusively due to , which was the main primary producer at lower temperatures. Two other CO fixation pathways were active at certain times and temperatures as indicated by transcripts: 3-hydroxypropionate (3-HP) bi-cycle due to and 3-hydroxypropionate-4-hydroxybutyrate (HH) cycle carried out by . The active transcription of the genes involved in these C-fixation pathways correlated with high determined carbon fixation rates. measurements of ammonia assimilation and nitrogen fixation (exclusively attributed to and mostly to sp.) showed these were the most important nitrogen acquisition pathways at 58 and 48°C. At 66°C ammonia oxidation genes were actively transcribed (mostly due to ). Reads indicated that denitrification was present as a nitrogen sink at all temperatures and that dissimilatory nitrate reduction to ammonia (DNRA) contributed very little. The combination of metagenomic and metatranscriptomic analysis with assimilation rates, allowed the reconstruction of day and night carbon and nitrogen assimilation pathways together with the contribution of keystone microorganisms in this natural hot spring microbial mat.
Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H13CO3) and nitrogen (15NH4Cl and K15NO3) assimilation rates. The microbial mat community included 31 phyla, of which only Cyanobacteria and Chloroflexi were dominant. At 58°C both phyla co-occurred, with similar contributions in relative abundances in metagenomes and total transcriptional activity. At 66°C, filamentous anoxygenic phototrophic Chloroflexi were >90% responsible for the total transcriptional activity recovered, while Cyanobacteria contributed most metagenomics and metatranscriptomics reads at 48°C. According to such reads, phototrophy was carried out both through oxygenic photosynthesis by Cyanobacteria (mostly Mastigocladus) and anoxygenic phototrophy due mainly to Chloroflexi. Inorganic carbon assimilation through the Calvin-Benson cycle was almost exclusively due to Mastigocladus, which was the main primary producer at lower temperatures. Two other CO2 fixation pathways were active at certain times and temperatures as indicated by transcripts: 3-hydroxypropionate (3-HP) bi-cycle due to Chloroflexi and 3-hydroxypropionate-4-hydroxybutyrate (HH) cycle carried out by Thaumarchaeota. The active transcription of the genes involved in these C-fixation pathways correlated with high in situ determined carbon fixation rates. In situ measurements of ammonia assimilation and nitrogen fixation (exclusively attributed to Cyanobacteria and mostly to Mastigocladus sp.) showed these were the most important nitrogen acquisition pathways at 58 and 48°C. At 66°C ammonia oxidation genes were actively transcribed (mostly due to Thaumarchaeota). Reads indicated that denitrification was present as a nitrogen sink at all temperatures and that dissimilatory nitrate reduction to ammonia (DNRA) contributed very little. The combination of metagenomic and metatranscriptomic analysis with in situ assimilation rates, allowed the reconstruction of day and night carbon and nitrogen assimilation pathways together with the contribution of keystone microorganisms in this natural hot spring microbial mat.Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were analyzed using metagenomics, metatranscriptomics and isotopically labeled carbon (H13CO3) and nitrogen (15NH4Cl and K15NO3) assimilation rates. The microbial mat community included 31 phyla, of which only Cyanobacteria and Chloroflexi were dominant. At 58°C both phyla co-occurred, with similar contributions in relative abundances in metagenomes and total transcriptional activity. At 66°C, filamentous anoxygenic phototrophic Chloroflexi were >90% responsible for the total transcriptional activity recovered, while Cyanobacteria contributed most metagenomics and metatranscriptomics reads at 48°C. According to such reads, phototrophy was carried out both through oxygenic photosynthesis by Cyanobacteria (mostly Mastigocladus) and anoxygenic phototrophy due mainly to Chloroflexi. Inorganic carbon assimilation through the Calvin-Benson cycle was almost exclusively due to Mastigocladus, which was the main primary producer at lower temperatures. Two other CO2 fixation pathways were active at certain times and temperatures as indicated by transcripts: 3-hydroxypropionate (3-HP) bi-cycle due to Chloroflexi and 3-hydroxypropionate-4-hydroxybutyrate (HH) cycle carried out by Thaumarchaeota. The active transcription of the genes involved in these C-fixation pathways correlated with high in situ determined carbon fixation rates. In situ measurements of ammonia assimilation and nitrogen fixation (exclusively attributed to Cyanobacteria and mostly to Mastigocladus sp.) showed these were the most important nitrogen acquisition pathways at 58 and 48°C. At 66°C ammonia oxidation genes were actively transcribed (mostly due to Thaumarchaeota). Reads indicated that denitrification was present as a nitrogen sink at all temperatures and that dissimilatory nitrate reduction to ammonia (DNRA) contributed very little. The combination of metagenomic and metatranscriptomic analysis with in situ assimilation rates, allowed the reconstruction of day and night carbon and nitrogen assimilation pathways together with the contribution of keystone microorganisms in this natural hot spring microbial mat.
Author Alcamán-Arias, María E.
Fernández, Camila
Díez, Beatriz
Pérez-Pantoja, Danilo
Pedrós-Alió, Carlos
Tamames, Javier
Vásquez, Mónica
AuthorAffiliation 3 Center for Climate and Resilience Research, Universidad de Chile , Santiago , Chile
2 Department of Molecular Genetics and Microbiology, Pontificia Universidad Católica de Chile , Santiago , Chile
5 Laboratoire d’Océanographie Microbienne, Observatoire Océanologique, Sorbonne Universités, Université Pierre-et-Marie-Curie, Centre National de la Recherche Scientifique , Banyuls-sur-Mer , France
6 Fondap IDEAL, Universidad Austral de Chile , Valdivia , Chile
1 Department of Oceanography, Universidad de Concepción , Concepción , Chile
4 Programa de Biología de Sistemas, Centro Nacional de Biotecnología – Consejo Superior de Investigaciones Científicas , Madrid , Spain
7 Programa Institucional de Fomento a la Investigación, Desarrollo e Innovación, Universidad Tecnológica Metropolitana , Santiago , Chile
AuthorAffiliation_xml – name: 1 Department of Oceanography, Universidad de Concepción , Concepción , Chile
– name: 3 Center for Climate and Resilience Research, Universidad de Chile , Santiago , Chile
– name: 7 Programa Institucional de Fomento a la Investigación, Desarrollo e Innovación, Universidad Tecnológica Metropolitana , Santiago , Chile
– name: 4 Programa de Biología de Sistemas, Centro Nacional de Biotecnología – Consejo Superior de Investigaciones Científicas , Madrid , Spain
– name: 2 Department of Molecular Genetics and Microbiology, Pontificia Universidad Católica de Chile , Santiago , Chile
– name: 6 Fondap IDEAL, Universidad Austral de Chile , Valdivia , Chile
– name: 5 Laboratoire d’Océanographie Microbienne, Observatoire Océanologique, Sorbonne Universités, Université Pierre-et-Marie-Curie, Centre National de la Recherche Scientifique , Banyuls-sur-Mer , France
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Copyright © 2018 Alcamán-Arias, Pedrós-Alió, Tamames, Fernández, Pérez-Pantoja, Vásquez and Díez. 2018 Alcamán-Arias, Pedrós-Alió, Tamames, Fernández, Pérez-Pantoja, Vásquez and Díez
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Keywords carbon and nitrogen assimilation
neutral hot spring
metatranscriptomics
photosynthesis
metagenomics
Cyanobacteria
microbial mat
Language English
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This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Microbiology
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Snippet Composition, carbon and nitrogen uptake, and gene transcription of microbial mat communities in Porcelana neutral hot spring (Northern Chilean Patagonia) were...
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SubjectTerms Biodiversity and Ecology
carbon and nitrogen assimilation
Cyanobacteria
Environmental Sciences
metagenomics
metatranscriptomics
microbial mat
Microbiology
neutral hot spring
Title Diurnal Changes in Active Carbon and Nitrogen Pathways Along the Temperature Gradient in Porcelana Hot Spring Microbial Mat
URI https://www.ncbi.nlm.nih.gov/pubmed/30333812
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