Thermogenic hydrocarbons fuel a redox stratified subseafloor microbiome in deep sea cold seep sediments

Abstract

20At marine cold seeps, gaseous and liquid hydrocarbons migrate from deep subsurface 21 origins to the sediment-water interface. Cold seep sediments are known to host 22CoM reductase pathway), longer-chain alkanes (fumarate addition pathway), and 35 aromatic hydrocarbons (fumarate addition and subsequent benzoyl-CoA pathways), 36 including novel lineages within Methanosarcinales and Chloroflexi. Geochemical 37 profiling demonstrated that hydrocarbon substrates are abundant in this location, 38 thermogenic in origin, and subject to biodegradation. The detection of alkyl-39 /arylalkylsuccinate metabolites, together with carbon isotopic signatures of ethane, 40propane and carbon dioxide, support that microorganisms are actively degrading 41 hydrocarbons in these sediments. Capacities for reductive dehalogenation, sulfide 42 oxidation, hydrogen oxidation, carbon fixation, and fermentation are also widespread. 43Most community members may indirectly benefit from thermogenic hydrocarbons 44 through interspecies transfer of electrons and metabolites, and degradation of 45 necromass. Thus, we conclude that upward migrated thermogenic hydrocarbons are 46 important carbon and energy sources that sustain diverse subseafloor microbial 47 communities at permanently cold hydrocarbon seeps. 48 3 Introduction 49 Marine cold seeps are characterised by the migration of gas and oil from deep 50 subsurface sources to the sediment-water interface 1, 2 . This seepage often contains 51 gaseous short-chain alkanes, as well as heavier liquid alkanes and aromatic 52 compounds 3 , that originate from deep thermogenic petroleum deposits. Migrated 53 hydrocarbons can serve as an abundant source of carbon and energy for 54 microorganisms in these ecosystems, either via their direct utilization or indirectly 55 through metabolizing by-products of hydrocarbon biodegradation 4 . Multiple 16S rRNA 56 gene surveys have revealed that cold seep sediments at or near the sediment-water 57 interface host an extensive diversity of archaeal and bacterial lineages 5-9 . However, 58 much less is known about metabolic versatility of this diverse microbiome, and how 59 surface and subsurface populations are connected and differentiated in different redox 60 zones within the sediment column 10, 11 . Most seep-associated microorganisms lack 61 sequenced genomes, precluding meaningful predictions of relationships between 62 microbial lineages and their biogeochemical functions 4, 8, 10-13 . 63 Geochemical studies have provided evidence that microorganisms in deep seafloor 64 sediments, including cold seeps, mediate anaerobic hydrocarbon oxidation 2, 3 . A range 65 of efforts have been undertaken to enrich and isolate anaerobic hydrocarbon-oxidizing 66 microorganisms from cold seep sediments and other ecosystems rich in hydrocarbons 67 (e.g. marine hydrothermal vents) [5][6][7][8][9] 14 . Numerous studies have focused on anaerobic 68 oxidation of methane, since methane generally is the dominant hydrocarbon in cold 69 seep fluids. This process is mediated by...

Distinct hydrogenotrophic bacteria are stimulated by elevated H2levels in upland and wetland soils

“…The taxonomy of each MAG was temporally assigned using GTDB-Tk [102] (GTDB R04-RS89 database). The relative abundance of each MAGs was calculated with CoverM (https://github.com/wwood/CoverM) as previously described [103]. The taxonomic classification, size, completeness, contamination, strain heterogeneity, and N50 of recovered MAGs are summarized in Table S4 .…”

Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

“…Except for EGM and SB, metagenomic datasets along with metadata were downloaded from NCBI Sequence Read Archive and NCBI BioSample databases (https://www.ncbi.nlm.nih.gov). Sample collection and DNA sequencing of samples from EGM and SB are described in detail elsewhere 23,24 .…”

Marine Sediments Harbor Diverse Archaea and Bacteria With Potentials for Anaerobic Hydrocarbon Degradation via Fumarate Addition

“…Apart from well-documented lineages of Deltaproteobacteria and Archaeoglobi [6,21], faeA genes are reported here as also occurring in the class Dehalococcoidia within the phylum Chloro exi, the class Thermoplasmata within the phylum Euryarchaeota, and within the Asgard superphylum (Lokiarchaeota, Thorarchaeota, and Heimdallarchaeota). Current knowledge about archaea involved in anaerobic hydrocarbon degradation focuses mainly on oxidation of methane and other short alkane gases using methyl-CoM reductase or methyl-CoM reductase-like enzymes [25,44,45]. New archaeal diversity presented here for the degradation of longer alkanes opens up a wider perspective on the evolution and expansion of hydrocarbon-oxidizing pathways throughout the archaeal domain.…”

“…Metagenomic analysis of a different oil reservoir revealed an Archaeoglobus encoding and expressing the alpha subunit of alkylsuccinate synthase (AssA) [22]. Investigations of marine sediments from cold seeps, hydrothermal elds and deep subsurface layers using genome-resolved metagenomics have revealed that hydrocarbon oxidizers that use fumarate addition might have an even wider phylogenetic distribution [23][24][25][26].…”