Microbial succession during the transition from active to inactive stages of deep-sea hydrothermal vent sulfide chimneys

Abstract

<jats:title>Abstract</jats:title> <jats:p>Background: Deep-sea hydrothermal vents are highly productive biodiversity hotspots in the deep ocean supported by chemosynthetic microorganisms. Prominent features of these systems are sulfide chimneys emanating high temperature hydrothermal fluids. While several studies have investigated the microbial diversity in both active and inactive sulfide chimneys that have been extinct for up to thousands of years, little is known about chimneys that have ceased activity more recently, as well as the microbial succession occurring during the transition from active to inactive chimneys. Results: Genome-resolved metagenomics was applied to an active and a recently extinct (~7 years) sulfide chimney from the 9°-10°N hydrothermal vent field on the East Pacific Rise. Full-length 16S rRNA gene and a total of 173 high quality metagenome assembled genomes (MAGs) were retrieved for comparative analysis. In the active chimney (L-vent), sulfide- and/or hydrogen-oxidizing Campylobacteria and Aquificae with the potential for denitrification were identified as the dominant community members and primary producers, fixing carbon through the reductive tricarboxylic acid (rTCA) cycle. In contrast, the microbiome of the recently extinct chimney (M-vent) was largely composed of heterotrophs from various bacterial phyla, including Delta -/ Beta -/ Alphaproteobacteria and Bacteroidetes . Gammaproteobacteria were identified as the main primary producers, using the oxidation of metal sulfides and/or iron oxidation coupled to nitrate reduction to fix carbon through the Calvin-Benson-Bassham (CBB) cycle. Further analysis revealed a phylogenetically distinct Nitrospirae cluster that has the potential to oxidize sulfide minerals coupled to oxygen and/or nitrite reduction, as well as for sulfate reduction, and that might serve as an indicator for the early stages of chimneys after venting has ceased. Conclusions: This study sheds light on the composition, metabolic functions, and succession of microbial communities inhabiting deep-sea hydrothermal vent sulfide chimneys. Collectively, microbial succession during the life span of a chimney could be described to proceed from a “fluid-shaped” microbial community in newly formed and actively venting chimneys supported by the oxidation of reductants in the hydrothermal fluid to a “mineral-shaped” community supported by the oxidation of minerals after hydrothermal activity has ceased. Remarkably, the transition appears to occur within the first few years, after which the communities stay stable for thousands of years.</jats:p>

Characterization of Sulfurimonas hydrogeniphila sp. nov., a Novel Bacterium Predominant in Deep-Sea Hydrothermal Vents and Comparative Genomic Analyses of the Genus Sulfurimonas

“…Furthermore, metagenomic and metatranscriptomic analyses revealed the processes and activities involving sulfur/hydrogen oxidation, oxygen respiration and denitrification as well as carbon fixation in genus Sulfurimonas inhabiting in vent fluids of Axial Seamount (Fortunato and Huber, 2016). These metabolic pathways were also observed in other hydrothermal samples such as actively venting chimney of East Pacific Rise and hydrothermal chimneys from the Roman Ruins vent field based on metagenomic and metaproteomic analyses (Pjevac et al, 2018;Hou et al, 2020).…”

Shaping of the Present-Day Deep Biosphere at Chicxulub by the Impact Catastrophe That Ended the Cretaceous

“…The deep subsurface microbiome below the Chicxulub impact crater was dominated by Proteobacteria, Bacteroidota, Firmicutes, and Actinobacteria, similar to predominant microbial communities associated with deep subsurface igneous rocks such as basalt, granite, volcanic glass, and inactive hydrothermal vents ( Jørgensen and Zhao, 2016 ; Zhang et al, 2016 ; Dutta et al, 2018 ; Hou et al, 2020 ). Despite a seemingly unequal downcore distribution of the ASVs, ordination and statistical analysis revealed that each lithology (postimpact, suevite, and granite) hosted a significantly different microbial community.…”

Keystone Genes Confer Superior Performance in Hyperthermophilic Composting

“…These results were in accordance with our nding that the relative abundance of the genus Bacillus, a strongly ammonifying taxon [44], was lower in hTC (Additional le 1, Figure S7). This shift may re ect the adaptation of microbial communities in hTC to hyperthermophilic conditions over time [45,46]. were decreased in hTC (Additional le 1, Table S2), and NC was increased (Additional le 1, Figure S1).…”

“…Statistical tests of genes involved in C degradation and N cycling in the two metagenomes were performed by pairwise comparisons of their abundances by using two-sided Fisher's exact test with con dence intervals at 95% signi cance using the Benjamini-Hochberg FDR multiple test correction in STAMP [45]. Random forest linear regression models were used to assess the accuracy of the random forest predictions for composting performance indices; R 2 and slope values closer to 1 indicate better models [29].…”