Abstract
ABSTRACTA considerable fraction of organic matter derived from photosynthesis in the euphotic zone settles into the ocean’s interior and, as it progresses, is degraded by diverse microbial consortia that utilize a suite of extracellular enzymes and membrane transporters. Still, the molecular details that regulate carbon cycling across depths remain little explored. As stratification in fjords has made them attractive models to explore patterns in biological oceanography, we here analyzed bacterial and archaeal transcription in samples from five depth layers in the Gullmar Fjord, Sweden. Transcriptional variation over depth correlated with gradients in chlorophyll a and nutrient concentrations. Differences in transcription between sampling dates (summer and early autumn) were strongly correlated with ammonium concentrations, which potentially was linked with a stronger influence of (micro-)zooplankton grazing in summer. Transcriptional investment in carbohydrate-active enzymes (CAZymes) decreased with depth and shifted toward peptidases, partly a result of elevated CAZyme transcription by Flavobacteriales, Cellvibrionales, and Synechococcales at 2 to 25 m and a dominance of peptidase transcription by Alteromonadales and Rhodobacterales from 50 m down. In particular, CAZymes for chitin, laminarin, and glycogen were important. High levels of transcription of ammonium transporter genes by Thaumarchaeota at depth (up to 18% of total transcription), along with the genes for ammonia oxidation and CO2 fixation, indicated that chemolithoautotrophy contributed to the carbon flux in the fjord. The taxon-specific expression of functional genes for processing of the marine pool of dissolved organic matter and inorganic nutrients across depths emphasizes the importance of different microbial foraging mechanisms over spatiotemporal scales for shaping biogeochemical cycles.IMPORTANCE It is generally recognized that stratification in the ocean strongly influences both the community composition and the distribution of ecological functions of microbial communities, which in turn are expected to shape the biogeochemical cycling of essential elements over depth. Here, we used metatranscriptomics analysis to infer molecular detail on the distribution of gene systems central to the utilization of organic matter in a stratified marine system. We thereby uncovered that pronounced shifts in the transcription of genes encoding CAZymes, peptidases, and membrane transporters occurred over depth among key prokaryotic orders. This implies that sequential utilization and transformation of organic matter through the water column is a key feature that ultimately influences the efficiency of the biological carbon pump.
Highlights
IMPORTANCE It is generally recognized that stratification in the ocean strongly influences both the community composition and the distribution of ecological functions of microbial communities, which in turn are expected to shape the biogeochemical cycling of essential elements over depth
The hydrolysis of high-molecular-weight dissolved organic matter (HMW-DOM) is considered the rate-limiting step in the marine carbon cycle [12], and bacteria secrete hydrolytic enzymes to utilize particulate organic matter and biopolymers [13], e.g., carbohydrate-active enzymes (CAZymes) and peptidases (PEPs), which cleave HMW-DOM into molecules smaller than ;600 Da that can be transported through the cell membrane [14]
The surface salinity in July was 28 practical salinity units (PSU) and decreased to 22 PSU in September and at both times increased with depth to ;36 PSU at 100 m (Fig. 1D), which corresponds to North Sea values [23]
Summary
IMPORTANCE It is generally recognized that stratification in the ocean strongly influences both the community composition and the distribution of ecological functions of microbial communities, which in turn are expected to shape the biogeochemical cycling of essential elements over depth. We thereby uncovered that pronounced shifts in the transcription of genes encoding CAZymes, peptidases, and membrane transporters occurred over depth among key prokaryotic orders This implies that sequential utilization and transformation of organic matter through the water column is a key feature that influences the efficiency of the biological carbon pump. Major portions of the primary production in the photic zone—up to ;40% of the photosynthetically fixed carbon—is transported vertically in the form of particulate organic matter into the ocean’s interior in a process referred to as the biological carbon pump [1]. Stratification thereby strongly influences both the microbial community composition and the ecological function of these communities [4] This is, for example, visible in the replacement of phototrophy genes dominating in surface waters by chemolithoautotrophy genes at depth [5,6,7,8,9]. We hypothesized that potential divergence in CAZyme, PEP, and transporter expression would be associated with shifts in dominance of transcription levels among taxa across depths
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