Novel Large Sulfur Bacteria in the Metagenomes of Groundwater-Fed Chemosynthetic Microbial Mats in the Lake Huron Basin

Abstract

Little is known about large sulfur bacteria (LSB) that inhabit sulfidic groundwater seeps in large lakes. To examine how geochemically relevant microbial metabolisms are partitioned among community members, we conducted metagenomic analysis of a chemosynthetic microbial mat in the Isolated Sinkhole, which is in a deep, aphotic environment of Lake Huron. For comparison, we also analyzed a white mat in an artesian fountain that is fed by groundwater similar to Isolated Sinkhole, but that sits in shallow water and is exposed to sunlight. De novo assembly and binning of metagenomic data from these two communities yielded near complete genomes and revealed representatives of two families of LSB. The Isolated Sinkhole community was dominated by novel members of the Beggiatoaceae that are phylogenetically intermediate between known freshwater and marine groups. Several of these Beggiatoaceae had 16S rRNA genes that contained introns previously observed only in marine taxa. The Alpena fountain was dominated by populations closely related to Thiothrix lacustris and an SM1 euryarchaeon known to live symbiotically with Thiothrix spp. The SM1 genomic bin contained evidence of H2-based lithoautotrophy. Genomic bins of both the Thiothrix and Beggiatoaceae contained genes for sulfur oxidation via the rDsr pathway, H2 oxidation via Ni-Fe hydrogenases, and the use of O2 and nitrate as electron acceptors. Mats at both sites also contained Deltaproteobacteria with genes for dissimilatory sulfate reduction (sat, apr, and dsr) and hydrogen oxidation (Ni-Fe hydrogenases). Overall, the microbial mats at the two sites held low-diversity microbial communities, displayed evidence of coupled sulfur cycling, and did not differ largely in their metabolic potentials, despite the environmental differences. These results show that groundwater-fed communities in an artesian fountain and in submerged sinkholes of Lake Huron are a rich source of novel LSB, associated heterotrophic and sulfate-reducing bacteria, and archaea.

Cellular reductase activity in uncultivatedThiomargarita spp. assayed using a redox-sensitive dye

“…35Flor, the genomes of Ca. T. nelsonii Thio36, and Bud S10 both contain genes for Ni-Fe hydrogenase (17, 18), as do those of other sulfur-oxidizing bacteria (36, 37). The source of H 2 to Thiomargarita in nature is not clear, but fermentation by epibionts or other bacteria in the environment is a possible source.…”

Geological degassing enhances microbial metabolism in the continental subsurface

“…2B), which seems to be a specific adaptation to hydrogen containing gases from the mantle. This class of hydrogenases was so far only detected in organisms of the Alti-2 group 14 and in an Alti-1 genome from the Alpena Fountain 35 . Additionally, Altiarchaeota employ a strictly anaerobic metabolism with only few members possessing an oxygen stress response system 12 , likely not enabling them to be aerobically dispersed across larger distances.…”

“…Altiarchaeota can be divided into two clusters, Alti-1 and Alti-2, with the latter having a broader metabolic variability than Alti-1 14 . However, organisms of the Alti-1 cluster are those that can dominate entire ecosystems, as shown for multiple ecosystems across the globe 12,5,35,13 . We investigated the metabolic capacities of the newly recovered Altiarchaeum GA genome in comparison with other Altiarchaeota ( Fig.…”

Genome-informed microscopy reveals infections of uncultivated carbon-fixing archaea by lytic viruses in Earth’s crust

“…To investigate Altiarchaeota-virus relationships, we explored ecosystems where Altiarchaeota comprised the majority of the community. Therefore, metagenomic data from a microbial mat growing in the sulfidic groundwater-fed Alpena County Library Fountain (ACLF) (Alpena, MI, USA) were obtained from NCBI Sequence Read Archive (SRA) repository [45] as were metagenome samples from Horonobe Underground Research Laboratory at 140 and 250 m depth (HURL, Hokkaido, Japan) [21]. The analysis was complemented with three metagenomic datasets from CO2-enriched groundwater erupted from a cold-water Geyser (Andernach, Middle Rhine Valley, Germany) [46], and the metagenome of a sulfidic spring Mühlbacher Schwefelquelle Isling (MSI) in Regensburg, Germany [7].…”