Complex Microbial Communities Drive Iron and Sulfur Cycling in Arctic Fjord Sediments

Abstract

Glacial retreat is changing biogeochemical cycling in the Arctic, where glacial runoff contributes iron for oceanic shelf primary production. We hypothesize that in Svalbard fjords, microbes catalyze intense iron and sulfur cycling in loworganic-matter sediments. This is because low organic matter limits sulfide generation, allowing iron mobility to the water column instead of precipitation as iron monosulfides. In this study, we tested this with high-depth-resolution 16S rRNA gene libraries in the upper 20 cm at two sites in Van Keulenfjorden, Svalbard. At the site closer to the glaciers, iron-reducing Desulfuromonadales, iron-oxidizing Gallionella and Mariprofundus, and sulfur-oxidizing Thiotrichales and Epsilonproteobacteria were abundant above a 12-cm depth. Below this depth, the relative abundances of sequences for sulfate-reducing Desulfobacteraceae and Desulfobulbaceae increased. At the outer station, the switch from iron-cycling clades to sulfate reducers occurred at shallower depths (ϳ5 cm), corresponding to higher sulfate reduction rates. Relatively labile organic matter (shown by ␦ 13 C and C/N ratios) was more abundant at this outer site, and ordination analysis suggested that this affected microbial community structure in surface sediments. Network analysis revealed more correlations between predicted iron-and sulfur-cycling taxa and with uncultured clades proximal to the glacier. Together, these results suggest that complex microbial communities catalyze redox cycling of iron and sulfur, especially closer to the glacier, where sulfate reduction is limited due to low availability of organic matter. Diminished sulfate reduction in upper sediments enables iron to flux into the overlying water, where it may be transported to the shelf. IMPORTANCE Glacial runoff is a key source of iron for primary production in the Arctic. In the fjords of the Svalbard archipelago, glacial retreat is predicted to stimulate phytoplankton blooms that were previously restricted to outer margins. Decreased sediment delivery and enhanced primary production have been hypothesized to alter sediment biogeochemistry, wherein any free reduced iron that could potentially be delivered to the shelf will instead become buried with sulfide generated through microbial sulfate reduction. We support this hypothesis with sequencing data that showed increases in the relative abundance of sulfate reducing taxa and sulfate reduction rates with increasing distance from the glaciers in Van Keulenfjorden, Svalbard. Community structure was driven by organic geochemistry, suggesting that enhanced input of organic material will stimulate sulfate reduction in interior fjord sediments as glaciers continue to recede.

Glacial runoff promotes deep burial of sulfur cycling-associated microorganisms in marine sediments

“…Lack of sulfide accumulation with depth indicated immediate re-oxidation and/or scavenging of sulfide produced from high sulfate reduction activity (Figure 1) (Wehrmann et al, 2017). In agreement with previous studies (Bourgeois et al, 2016; Buongiorno et al, 2019; Park et al, 2011), differences in organic matter availability and electron acceptor concentrations are suggested to had a major influence on the composition of the seafloor microbial community in glaciated fjords.…”

“…Arctic fjords with marine-terminating glaciers constitute an important interface for freshwater and sediment influx from land into the sea, thereby influencing the physical and chemical conditions in the coastal marine ecosystems (Etherington et al, 2007; Svendsen et al, 2002). The high influx of sedimentary materials, e.g., minerals, terrigenous organic matter and metals, in glacier-associated fjords has a strong effect on the distributions of the benthic microbial communities (Bourgeois et al, 2016; Buongiorno et al, 2019; Park et al, 2011). Increased water turbidity in close proximity to the glacier can negatively influence surface water primary production (Etherington et al, 2007; Zajączkowski, 2008), which leads to lower organic matter availability in the underlying sediments (Bourgeois et al, 2016).…”

“…Of prime importance in microbial organic matter degradation is the respiratory reduction of sulfate to sulfide, which facilitates up to 69% of the total organic matter mineralization in Arctic fjord sediments (Sørensen et al, 2015). Other key electron acceptors are metals such as iron(oxyhydr)oxides and manganese oxides that can be introduced in high amounts via glacial runoff to marine sediments and are subjected to redox cycling (Bhatia et al, 2013; Buongiorno et al, 2019; Laufer et al, 2016; Wehrmann et al, 2014). Fe(III) and Mn(IV) also facilitate the oxidation of reduced sulfur compounds (Wehrmann et al, 2014; Zopfi et al, 2004) and thereby fuel a cryptic sulfur cycle in glacier-influenced sediments (Wehrmann et al, 2017).…”

Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

“…Sites within Van Keulenfjorden (sites AB and AC) and Kongsfjorden (sites P and F), Svalbard, were investigated for their geochemical properties and relative abundance of Woeseiales with depth (Fig 1a-1c). Previous geochemical analysis on porewaters at these sites showed higher relative concentrations of Fe (up to~300 nM) at site AB compared to <50 nM at site AC in the top 5 cm of sediment [22]. Within shallow sediments at site AB, Mn concentrations never exceed 65 nM, while at site AC, Mn concentrations exceed 250 nM [22].…”

Transformation of organic matter in a Barents Sea sediment profile: coupled geochemical and microbiological processes

“…Seasonal or decadal oscillations in the delivery of OM causing the position of the redox boundary to fluctuate could be a process here, potentially explaining the position of Mn at the upper part of the redox boundary based on kinetics of oxidation and reduction [87]. The oxic to anoxic redox transition is most clearly illustrated by the marked increase of Desulforbacteraceae from ~10.5 cm downwards which are known sulfate reducers [88] and correlates with modeled sulfate reduction ( Fig. 3; Supplements Fig.…”