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Front. Microbiol. | doi: 10.3389/fmicb.2018.02353

Diurnal changes in active carbon and nitrogen pathways along the temperature gradient in Porcelana hot spring microbial mat

  • 1Oceanography, Universidad de Concepción, Chile
  • 2Molecular Genetics and Microbiologyy, Pontificia Universidad Católica de Chile, Chile
  • 3CR2, Universidad de Chile, Chile
  • 4Programa de Biología de Sistemas, Centro Nacional de Biotecnología (CNB), Spain
  • 5Laboratoire d'Océanographie Microbienne (LOMIC), UMS2348 Observatoire océanologique de Banyuls-sur-Mer (OOB), France
  • 6Fondap IDEAL, Universidad Austral de Chile, Chile
  • 7Programa Institucional de Fomento a la Investigación, Desarrollo e Innovación, Metropolitan University of Technology, Chile

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.

Keywords: Cyanobacteria, Carbon and nitrogen assimilation, neutral hot spring, Metagenomics, metatranscriptomics, microbial mat, Photosynthesis

Received: 22 Nov 2017; Accepted: 13 Sep 2018.

Edited by:

Ana B. Pacheco, Universidade Federal do Rio de Janeiro, Brazil

Reviewed by:

Luisa I. Falcon, Universidad Nacional Autónoma de México, Mexico
Vera Thiel, Tokyo Metropolitan University, Japan
Eric D. Becraft, University of North Alabama, United States  

Copyright: © 2018 Alcaman-Arias, Pedrós-Alió, Tamames, Fernández, Pérez-Pantoja, Vásquez and Díez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Beatriz Díez, Pontificia Universidad Católica de Chile, Molecular Genetics and Microbiologyy, Santiago, Chile,