Articles | Volume 13, issue 14
Biogeosciences, 13, 4135–4149, 2016

Special issue: Biogeochemical and biological response to a diazotroph bloom...

Biogeosciences, 13, 4135–4149, 2016

Research article 19 Jul 2016

Research article | 19 Jul 2016

Global analysis of gene expression dynamics within the marine microbial community during the VAHINE mesocosm experiment in the southwest Pacific

Ulrike Pfreundt1, Dina Spungin2, Sophie Bonnet3,4, Ilana Berman-Frank2, and Wolfgang R. Hess1 Ulrike Pfreundt et al.
  • 1Institute for Biology III, University of Freiburg, Freiburg, Germany
  • 2Mina and Everard Goodman Faculty of Life Sciences, Bar Ilan University, Ramat Gan, Israel
  • 3Aix Marseille Université, CNRS/INSU, Université de Toulon, IRD, Mediterranean Institute of Oceanography (MIO), Marseille, France
  • 4Institut de Recherche pour le Développement, AMU/ CNRS/INSU, Université de Toulon, Mediterranean Institute of Oceanography (MIO) Nouméa, New Caledonia, France

Abstract. Microbial gene expression was followed for 23 days within a mesocosm (M1) isolating 50 m3 of seawater and in the surrounding waters in the Nouméa lagoon, New Caledonia, in the southwest Pacific as part of the VAriability of vertical and tropHIc transfer of diazotroph derived N in the south wEst Pacific (VAHINE) experiment. The aim of VAHINE was to examine the fate of diazotroph-derived nitrogen (DDN) in a low-nutrient, low-chlorophyll ecosystem. On day 4 of the experiment, the mesocosm was fertilized with phosphate. In the lagoon, gene expression was dominated by the cyanobacterium Synechococcus, closely followed by Alphaproteobacteria. In contrast, drastic changes in the microbial community composition and transcriptional activity were triggered within the mesocosm within the first 4 days, with transcription bursts from different heterotrophic bacteria in rapid succession. The microbial composition and activity of the surrounding lagoon ecosystem appeared more stable, although following similar temporal trends as in M1. We detected significant gene expression from Chromerida in M1, as well as the Nouméa lagoon, suggesting these photoautotrophic alveolates were present in substantial numbers in the open water. Other groups contributing substantially to the metatranscriptome were affiliated with marine Euryarchaeota Candidatus Thalassoarchaea (inside and outside) and Myoviridae bacteriophages likely infecting Synechococcus, specifically inside M1. High transcript abundances for ammonium transporters and glutamine synthetase in many different taxa (e.g., Pelagibacteraceae, Synechococcus, Prochlorococcus, and Rhodobacteraceae) was consistent with the known preference of most bacteria for this nitrogen source. In contrast, Alteromonadaceae highly expressed urease genes; Rhodobacteraceae and Prochlorococcus showed some urease expression, too. Nitrate reductase transcripts were detected on day 10 very prominently in Synechococcus and in Halomonadaceae. Alkaline phosphatase was expressed prominently only between days 12 and 23 in different organisms, suggesting that the microbial community was not limited by phosphate, even before the fertilization on day 4, whereas the post-fertilization community was.

We observed high expression of the Synechococcus sqdB gene, only transiently lowered following phosphate fertilization. SqdB encodes UDP-sulfoquinovose synthase, possibly enabling marine picocyanobacteria to minimize their phosphorus requirements by substitution of phospholipids with sulphur-containing glycerolipids. This result suggests a link between sqdB expression and phosphate availability in situ.

Gene expression of diazotrophic cyanobacteria was mainly attributed to Trichodesmium and Richelia intracellularis (diatom–diazotroph association) in the Nouméa lagoon and initially in M1. UCYN-A (Candidatus Atelocyanobacterium) transcripts were the third most abundant and declined both inside and outside after day 4, consistent with 16S- and nifH-based analyses. Transcripts related to the Epithemia turgida endosymbiont and Cyanothece ATCC 51142 increased during the second half of the experiment.

Short summary
The VAHINE experiment in the New Caledonia lagoon (SW Pacific) targeted the dynamics of nutrient pools and fluxes, N2 fixation, and the composition and productivity of the microbial communities. To connect this information to the actual activities of diverse microbial taxa, we present the analysis of the community-wide gene expression for 23 days. The results from this experiment provide insight into the microbial activities in a low-nutrient, low-chlorophyll ecosystem and within a mesocosm.
Final-revised paper