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

Ulrike Pfreundt, Dina Spungin, Sophie Bonnet, Ilana Berman-Frank, Wolfgang R. Hess

Research output: Contribution to journalArticlepeer-review

Abstract

Microbial gene expression was followed for 23 days within a mesocosm (M1) isolating 50m3 of seawater and in the surrounding waters in the Noumeá 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 Noumeá 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 Noumeá 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.

Original languageEnglish
Pages (from-to)4135-4149
Number of pages15
JournalBiogeosciences
Volume13
Issue number14
DOIs
StatePublished - 19 Jul 2016
Externally publishedYes

Bibliographical note

Funding Information:
The authors thank the captain and crew of the R/V Alis for their great support during the cruise, to Eyal Rahav throughout the experimental campaign, to Brian Haas (The Broad Institute) and Ben Fulton (Indiana University) for their patient help with the Trinity de-novo transcriptome assembler, Craig Nelson (University of Hawaii at Manoa) for his valuable advice on multivariate statistics, Bj?rn Gr?ning (University of Freiburg) for his immediate actions regarding tool updates and bugs on the local Galaxy server, and Steffen Lott (University of Freiburg) for his help with the visualization tool CoVennTree. The participation of Ulrike Pfreundt, Wolfgang R. Hess, Dina Spungin, and Ilana Berman-Frank in the VAHINE experiment was supported by the German-Israeli Research Foundation (GIF), project number 1133-13.8/2011, the United States-Israel Binational Science Foundation (BSF) grant 2008048 to Ilana Berman-Frank and the metatranscriptome analysis by the EU project MaCuMBA (Marine Microorganisms: Cultivation Methods for Improving their Biotechnological Applications; grant agreement no. 311975) to Wolfgang R. Hess.

Publisher Copyright:
© 2016 Author(s).

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Earth-Surface Processes

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