Taxon-Specific Shifts in Bacterial and Archaeal Transcription of Dissolved Organic Matter Cycling Genes in a Stratified Fjord

• Published in: mSystems 2021-12, Vol.6 (6), p.e0057521-e0057521
• Main Authors: Pontiller, Benjamin, Pérez-Martínez, Clara, Bunse, Carina, Osbeck, Christofer M G, González, José M, Lundin, Daniel, Pinhassi, Jarone
• Format: Article
• Language: English
• Subjects: Akvatisk ekologi; Ammonia; Ammonium; Ammonium transporter; Aquatic Ecology; Bacteria; Biopolymers; carbohydrate-active enzymes; Carbon; Carbon cycle; Carbon dioxide; Carbon dioxide fixation; Chitin; Chlorophyll; Cluster analysis; Community composition; Cyanobacteria; dissolved organic carbon; Dissolved organic matter; Environmental Microbiology; Enzymes; Euphotic zone; Extracellular enzymes; fjord; Fjords; Glycogen; Laminarin; marine bacteria; metatranscriptomics; Microbiology; Mikrobiologi; Nitrosopumilus; Nutrient concentrations; Nutrients; Oceanography; Oxidation; Peptidase; peptidases; Photosynthesis; Research Article; Salinity; Stratification; Taxonomy; Transcription; transporters; vertical depth gradients; Water column; Zooplankton
• ISSN: 2379-5077; 2379-5077
• DOI: 10.1128/mSystems.00575-21

A 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 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 , , and at 2 to 25 m and a dominance of peptidase transcription by and from 50 m down. In particular, CAZymes for chitin, laminarin, and glycogen were important. High levels of transcription of ammonium transporter genes by at depth (up to 18% of total transcription), along with the genes for ammonia oxidation and CO 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. 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 mat