Abstract
Environmental microbial gene expression patterns remain largely unexplored, particularly at interannual time scales. We analyzed the variability in the expression of marker genes involved in ecologically relevant biogeochemical processes at a temperate Atlantic site over two consecutive years. Most of nifH transcripts, involved in nitrogen (N) fixation, were affiliated with the symbiotic cyanobacterium Candidatus Atelocyanobacterium thalassa, suggesting a key role as N providers in this system. The expression of nifH and amoA (i.e., marker for ammonia oxidation) showed consistent maxima in summer and autumn, respectively, suggesting a temporal succession of these important N cycling processes. The patterns of expression of genes related to the oxidation of carbon monoxide (coxL) and reduced sulfur (soxB) were different from that of amoA, indicating alternate timings for these energy conservation strategies. We detected expression of alkaline phosphatases, induced under phosphorus limitation, in agreement with the reported co-limitation by this nutrient at the study site. In contrast, low-affinity phosphate membrane transporters (pit) typically expressed under phosphorus luxury conditions, were mainly detected in post-bloom conditions. Rhodobacteraceae dominated the expression of soxB, coxL and ureases, while Pelagibacteraceae dominated the expression of proteorhodopsins. Bacteroidetes and Gammaproteobacteria were major contributors to the uptake of inorganic nutrients (pit and amt transporters). Yet, in autumn, Thauma- and Euryarchaeota unexpectedly contributed importantly to the uptake of ammonia and phosphate, respectively. We provide new hints on the active players and potential dynamics of ecologically relevant functions in situ, highlighting the potential of metatranscriptomics to provide significant input to future omics-driven marine ecosystem assessment.
Highlights
The analysis of marine protein-coding genes has undergone rapid expansion following the development of meta-omics technologies and its application to oceanic environments, from local to large-scale ocean surveys (Gilbert and Dupont, 2011; Moran et al, 2013; Salazar et al, 2019)
As compared to the oceanic distribution of these functional marker genes, our knowledge on their gene expression patterns has grown at a slower pace
Our aims were (i) to identify key biogeochemical pathways that were active at the study site by following the expression dynamics of functional marker genes, (ii) to analyze the composition of transcriptionally active taxa involved in these functions, and (iii) to understand the variability in their expression levels under environmental conditions ranging from oligotrophic to mesotrophic, as typically found in temperate waters over the seasonal cycle
Summary
The analysis of marine protein-coding genes has undergone rapid expansion following the development of meta-omics technologies and its application to oceanic environments, from local to large-scale ocean surveys (Gilbert and Dupont, 2011; Moran et al, 2013; Salazar et al, 2019). Gene Expression Patterns of Coastal Microorganisms new perspectives on the ocean biogeochemistry, including the discovery of novel enzymes, pathways, and key microbial players (Zehr and Kudela, 2011; Ferrera et al, 2015) In this regard, the identification of marker genes, highly specific for some metabolic functions, has been key to address the abundance, diversity and geographic extent of microbes involved in biogeochemically relevant processes, such as nitrification (amoA genes, Francis et al, 2005; Sintes et al, 2013), nitrogen fixation (nifH genes; Zehr et al, 2003), or carbon monoxide oxidation (cox genes; King and Weber, 2007). While the production of DMS from DMSP was first described in Rhodobacteraceae, other key players in this process, such as some members of Gammaproteobacteria, have been identified by experimental metatranscriptomics (Vila-Costa et al, 2010)
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