Microbial iron metabolism as revealed by gene expression profiles in contrasted Southern Ocean regimes

Abstract

Summary Iron (Fe) is a limiting nutrient in large regions of the ocean, but the strategies of prokaryotes to cope with this micronutrient are poorly known. Using a gene‐specific approach from metatranscriptomics data, we investigated seven Fe‐related metabolic pathways in microbial communities from high nutrient low chlorophyll and naturally Fe‐fertilized waters in the Southern Ocean. We observed major differences in the contribution of prokaryotic groups at different taxonomic levels to transcripts encoding Fe‐uptake mechanisms, intracellular Fe storage and replacement and Fe‐related pathways in the tricarboxylic acid (TCA) cycle. The composition of the prokaryotic communities contributing to the transcripts of a given Fe‐related pathway was overall independent of the in situ Fe supply, indicating that microbial taxa utilize distinct Fe‐related metabolic processes. Only a few prokaryotic groups contributed to the transcripts of more than one Fe‐uptake mechanism, suggesting limited metabolic versatility. Taxa‐specific expression of individual genes varied among prokaryotic groups and was substantially higher for all inspected genes in Fe‐limited as compared to naturally fertilized waters, indicating the link between transcriptional state and Fe regime. Different metabolic strategies regarding low Fe concentrations in the Southern Ocean are discussed for two abundant prokaryotic groups, Pelagibacteraceae and Flavobacteriaceae .

Seasonal dynamics of prokaryotes and their associations with diatoms in the Southern Ocean as revealed by an autonomous sampler

“…Aerobic heterotrophic microbes can couple nitrite oxidation to energy conservation while relying on organic matter for growth (Kuypers et al ., 2018). Nitrification processes are associated with high iron requirements, which appear to be met by both the iron supply (Blain et al ., 2007; Sarthou et al ., 2008) and the metabolic capability for the uptake of Fe 3+ and siderophore‐bound iron (Debeljak et al ., 2019). Based on seasonal changes in nitrate concentrations, uptake rates, and the decoupling between N and O isotopes, Fripiat et al .…”

“…Using MICRO‐CARD‐FISH and 55 Fe, Gammaproteobacteria and FCB dominated iron uptake in spring (Fourquez et al ., 2016). Cellvibrionaceae (SAR92) and Flavobacteriaceae contributed each 10%–15% to total prokaryotic siderophore‐bound iron uptake gene expression, while the contribution of Nitrincolaceae (formerly Oceanospirillaceae ), a bacterial group that appeared later in the season (see below) was lower (5%) (Debeljak et al ., 2019). Collectively, these observations illustrate the metabolic potential of these groups for the rapid utilization of major compounds comprised of diatom‐derived DOM coupled to efficient iron uptake strategies.…”

“…Their increased contribution could therefore reflect changes in the DOM composition over time. In addition, RCA representatives from Antarctic waters have distinct iron uptake and metabolism strategies (Sun et al ., 2017), in line with observations from early spring when Rhodobacteraceae accounted for 5%–10% of total Fe 2+ and Fe 3+ uptake transcripts (Debeljak et al ., 2019).…”

High contribution ofPelagibacteralesto bacterial community composition and activity in spring blooms off Kerguelen Island (Southern Ocean)

“…While SAR11 cells were major contributors to leucine incorporation, they were less adapted at taking up more complex compounds such as chitin (Fourquez et al , 2016). The success of SAR11 in these Fe-limited waters could further be due to strategies related to uptake, storage and utilization of this micronutrient (Debeljak et al , 2019; Beier et al , 2015).…”

Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph Alteromonas macleodii

“…have been found to become highly abundant in environments enriched in organic matter and nutrients (22)(23)(24)(25)(26). Observations of Southern Ocean bacterial communities have also found Alteromonadaceae to contribute significantly to the pool of iron uptake transcripts in this system (27). As "first responders" to bloom events and other episodes of particle enrichment, Alteromonas spp.…”