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Temporal Dynamics of Active Prokaryotic Nitrifiers and Archaeal Communities from River to Sea

Abstract

To test if different niches for potential nitrifiers exist in estuarine systems, we assessed by pyrosequencing the diversity of archaeal gene transcript markers for taxonomy (16S ribosomal RNA (rRNA)) during an entire year along a salinity gradient in surface waters of the Charente estuary (Atlantic coast, France). We further investigated the potential for estuarine prokaryotes to oxidize ammonia and hydrolyze urea by quantifying thaumarchaeal amoA and ureC and bacterial amoA transcripts. Our results showed a succession of different nitrifiers from river to sea with bacterial amoA transcripts dominating in the freshwater station while archaeal transcripts were predominant in the marine station. The 16S rRNA sequence analysis revealed that Thaumarchaeota marine group I (MGI) were the most abundant overall but other archaeal groups like Methanosaeta were also potentially active in winter (December–March) and Euryarchaeota marine group II (MGII) were dominant in seawater in summer (April–August). Each station also contained different Thaumarchaeota MGI phylogenetic clusters, and the clusters’ microdiversity was associated to specific environmental conditions suggesting the presence of ecotypes adapted to distinct ecological niches. The amoA and ureC transcript dynamics further indicated that some of the Thaumarchaeota MGI subclusters were involved in ammonia oxidation through the hydrolysis of urea. Our findings show that ammonia-oxidizing Archaea and Bacteria were adapted to contrasted conditions and that the Thaumarchaeota MGI diversity probably corresponds to distinct metabolisms or life strategies.

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Acknowledgments

We thank P. Pineau, N. Lachaussée, M. Breret, F. Mornet, L. Beaugeard, J. Lavaud, and J. Jourde for the sampling. We thank A. Vellet, I. Louati, M. Breret, and C. Lavergne for their technical support during the experimentations and J.C. Auguet for providing us the map of the sampling location of the stations. This work was supported by a CNRS Program Ecosphère Continentale et Côtière (EC2CO, 2010–2012). The work of PE Galand was supported by the Agence Nationale de la Recherche (ANR) project MICADO (ANR-11JSV7-003-01).

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Correspondence to Isabelle Mary.

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Supplementary Figure 1
figure 6

Box plot of Shannon index from the three different sampling stations. A significant difference in diversity between two stations is marked with a star (*, p < 0.008) (GIF 23 kb)

Supplementary Figure 2
figure 7

Ordination diagram from CCA of major active archaeal groups compared with environmental data (GIF 28 kb)

ESM 3

(TIFF 25480 kb)

ESM 4

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Supplementary Table 1

Quality checked (QC) and Archaea affiliated sequences obtained for each sample from surface water collected monthly in the Charente estuary. Environmental parameters (temperature, salinity, pH, and Chla, ammonia and phosphates concentrations) associated to each point are presented. ND: not determined (XLS 43 kb)

Supplementary Table 2

Mean number of 16S rRNA sequences associated with each abundant OTU retrieved in the freshwater, mesohaline, and marine stations. ND: not determined (XLS 32 kb)

Supplementary Table 3

Monthly community structure at the subcluster level in Thaumarchaeota MGI. Number of OTUs were presented for each subgroup and number of sequences between brackets. ND: not determined (XLS 37 kb)

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Hugoni, M., Agogué, H., Taib, N. et al. Temporal Dynamics of Active Prokaryotic Nitrifiers and Archaeal Communities from River to Sea. Microb Ecol 70, 473–483 (2015). https://doi.org/10.1007/s00248-015-0601-z

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  • DOI: https://doi.org/10.1007/s00248-015-0601-z

Keywords

  • Ammonia oxidation
  • amoA
  • Archaea
  • Gradient
  • Diversity