Microbial community composition and functional potential in Bothnian Sea sediments is linked to Fe and S dynamics and the quality of organic matter

Abstract

The Bothnian Sea is an oligotrophic brackish basin characterized by low salinity and high concentrations of reactive iron, methane, and ammonium in its sediments, enabling the activity and interactions of many microbial guilds. Here, we studied the microbial network in these sediments by analyzing geochemical and microbial community depth profiles at one offshore and two near coastal sites. Analysis of 16S rRNA gene amplicons revealed a distinct depth stratification of both archaeal and bacterial taxa. The microbial communities at the two near coastal sites were more similar to each other than the offshore site, which is likely due to differences in the quality and rate of organic matter degradation. The abundance of methanotrophic archaea of the ANME-2a clade was shown to be related to the presence of methane and varied with sediment iron content. Metagenomic sequencing of sediment-derived DNA from below the sulfate-methane transition zone revealed a broad potential for respiratory sulfur metabolism via partially reduced sulfur species. The potential for nitrogen cycling was dominated by reductive processes via a truncated denitrification pathway encoded exclusively by bacterial lineages. Gene-centric fermentative metabolism analysis indicated a potential importance for acetate, formate, alcohol, and hydrogen metabolism. Methanogenic/-trophic pathways were dominated by Methanosaetaceae, Methanosarcinaceae, Methanomassiliicoccaceae, Methanoregulaceae, and ANME-2 archaea. Our results indicated flexible metabolic capabilities of core microbial community taxa, which could adapt to changing redox conditions, and with a spatial and depth distribution that is likely governed by the quality and input of available organic substrates and, for ANME-2, of iron oxides.

Influence of electron acceptor availability and microbial community structure on sedimentary methane oxidation in a boreal estuary

“…1 and 2). Furthermore, the same dominant methanogen taxa, Methanomicrobiales (Methanoregulaceae), Methanosaetaceae and Methanosarcinaceae, were present both at our study sites and in Bothnian Sea sediments (Rasigraf et al 2019) (Fig. 4).…”

“…reducing bacteria and conductive minerals such as in iron-rich sediments of our study sites, Methanosaetaceae and Methanosarcinaceae could also drive CO 2 -reduction (to CH 4 ) coupled with either direct or indirect (via conductive materials) electron transfer from iron-reducing bacteria, such as Geobacter (Rotaru et al 2014(Rotaru et al , 2018. Some metagenomic datasets also indicate Bathyarchaeota, which were dominant archaea both at our study sites and Bothnian Sea sediments (Rasigraf et al 2019) ( Supplementary Fig. 1), can be both methanogenic and methanotrophic (Evans et al 2015).…”

“…4). Although Rasigraf et al (2019) were able to construct a metagenome-assembled-genome of Methanomassiliicoccaceae thriving in Bothnian Sea sediments, this family, alongside other methanogenic taxa, were at very low levels both at ours and their study sites. Methanomicrobiales and Methanosaetaceae are considered to drive hydrogenotrophic and acetoclastic methanogenic pathways, respectively, while both acetoclastic and methylotrophic pathways have been suggested for Methanosarcinaceae (Nazaries et al 2013).…”

“…The sediment archaeal and bacterial communities at sites A and D generally consisted of the same taxa as in coastal and offshore sites of another northern Baltic Sea area, the Bothnian Sea (Rasigraf et al 2019) ( Supplementary Figs. 1 and 2).…”

“…Shotgun metagenomic data would be needed to assess genetic potential of Bathyarchaeota at our study sites. However, the metagenomes of Rasigraf et al (2019) suggest a non-methanogenic/non-methanotrophic fermentative lifestyle for Bathyarchaeota in Bothnian Sea sediments.…”