Uptake of Leucine, Chitin, and Iron by Prokaryotic Groups during Spring Phytoplankton Blooms Induced by Natural Iron Fertilization off Kerguelen Island (Southern Ocean)

Abstract

Iron and carbon are essential for microbial heterotrophic activity, but the bioavailability of these elements is low in surface waters of the Southern Ocean. Whether the access to iron and carbon differs among phylogenetic groups of prokaryotes is barely known. To address this question we used iron (55 FeCl 3), and the carbon compounds chitin (3 H-Diacetylchitobiose) and leucine (3 H-leucine) as model substrates in combination with MICRO-CARD-FISH during spring phytoplankton blooms induced by natural iron fertilization off Kerguelen Island (KErguelen Ocean and Plateau compared Study 2-KEOPS2; October-November 2011). The application of probes at broad phylogenetic levels indicated an overall similar community composition in surface waters at the 8 investigated sites. The relative contributions of the prokaryotic groups to abundance revealed a strong positive relationship with their respective contributions to the leucine-active community (p < 0.0001; r = 0.93). This relationship was much weaker for chitin (p < 0.001; r = 0.51) and absent for iron (p > 0.05; r = 0.26). These results suggest preferential uptake of iron and chitin by some prokaryotic groups. SAR11 and Cytophaga-Flavobacterium-Bacteroides (CFB) were the dominant contributors to the leucine-active community, while CFB and Archaea had the highest contributions to the chitin-active community. By contrast, Gammaproteobacteria, including SAR86, and CFB revealed the highest contributions to the iron-active community. We found several correlations between the group-specific fractions of active cells for a given substrate and most of them included CFB, pointing to the potential importance of microbial interactions for iron and carbon cycling in the Southern Ocean.

Major changes in the composition of a Southern Ocean bacterial community in response to diatom-derived dissolved organic matter

“…Flavobacteria are known to be efficient degraders of complex polymers, such as polysaccharides, proteins or chitin, and tend to be less active than other bacterial groups in taking up simple sugars or amino acids González et al 2008;Straza et al 2010;Simon et al 2012;Wietz et al 2015;Fourquez et al 2016). These characteristics are supported by proteomic and genomic studies showing that Flavobacteria possess numerous genes involved in hydrolytic activities as well as high molecular weight compounds transporters such as TonB-dependent receptors, and comparatively low numbers of genes involved in the uptake of low molecular weight compounds (González et al 2008;Gómez-Pereira et al 2012;Fernández-Gómez et al 2013;Williams et al 2013).…”

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

“…For the normalization step, we therefore assumed that the above‐mentioned ratio derived from qPCR data equals the ratio of SAR11‐isocitrate lyase gene transcripts (metatranscriptome; RNA) to the number of SAR11 cell per L estimated by CARD‐FISH (as described in the study by Fourquez et al . ): where, for the purpose of this study, qT iso /qC iso is the ratio of SAR11‐isocitrate lyase gene transcripts L −1 (qT iso ) to SAR11‐isocitrate lyase gene copies L −1 (qC iso ) estimated by qPCR (Beier et al ., ), mT iso is the number of SAR11‐isocitrate lyase gene transcripts L −1 , and nC SAR11 is the SAR11 cells L −1 estimated by CARD‐FISH (Fourquez et al . )…”

“…The OTUs were corrected for copy numbers of 16S rRNA gene per cell per specific taxa obtained from the ribosomal RNA database (Stoddard et al ., ). Total cell numbers per bacterial group were then calculated with 16S rRNA gene relative proportions and counts from the Eub228‐I, ‐II and ‐II catalysed reporter deposition–fluorescence in situ hybridization (CARD‐FISH) probe from the same samples (data from the study by Fourquez et al ., , Supporting Information Table S6).…”

Leucine, starch and bicarbonate utilization by specific bacterial groups in surface shelf waters off Galicia (NWSpain)

“…Although there is little experimental evidence about the capabilities of distinct bacterial populations to degrade polysaccharides in marine surface waters, some studies have shown the dominance of taxa belonging to the Gammaproteobacteria and/or Bacteroidetes groups in microcosms amended with starch, alginate or agarose (Simon et al, 2012;Wietz et al, 2015). By contrast, only members from the Bacteroidetes group seem to have a prominent role in the degradation of chitin (Wietz et al, 2015;Fourquez et al, 2016).…”

“…In contrast to the widely studied patterns of utilization of monomers at the single cell level, relatively few studies have examined macromolecule incorporation by specific marine microbes (Cottrell and Kirchman, 2000;Elifantz et al, 2005;Fourquez et al, 2016), documenting differences in incorporation at the phylum and class levels. To the best of our knowledge, the utilization of starch in natural communities has not yet been evaluated at a single-cell level.…”