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Helarchaeota and Co-Occurring Sulfate-Reducing Bacteria in Subseafloor

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Helarchaeota and Co-Occurring Sulfate-Reducing Bacteria in Subseafloor www.nature.com/ismecomms ARTICLE OPEN Helarchaeota and co-occurring sulfate-reducing bacteria in subseafloor sediments from the Costa Rica Margin ✉ Rui Zhao1 and Jennifer F. Biddle 1 © The Author(s) 2021 Deep sediments host many archaeal lineages, including the Asgard superphylum which contains lineages predicted to require syntrophic partnerships. Our knowledge about sedimentary archaeal diversity and their metabolic pathways and syntrophic partners is still very limited. We present here new genomes of Helarchaeota and the co-occurring sulfate-reducing bacteria (SRB) recovered from organic-rich sediments off Costa Rica Margin. Phylogenetic analyses revealed three new metagenome-assembled genomes (MAGs) affiliating with Helarchaeota, each of which has three variants of the methyl-CoM reductase-like (MCR-like) complex that may enable them to oxidize short-chain alkanes anaerobically. These Helarchaeota have no multi-heme cytochromes but have Group 3b and Group 3c [NiFe] hydrogenases, and formate dehydrogenase, and therefore have the capacity to transfer the reducing equivalents (in the forms of hydrogen and formate) generated from alkane oxidation to external partners. We also recovered five MAGs of SRB affiliated with the class of Desulfobacteria, two of which showed relative abundances (represented by genome coverages) positively correlated with those of the three Helarchaeota. Genome analysis suggested that these SRB bacteria have the capacity of H2 and formate utilization and could facilitate electron transfers from other organisms by means of these reduced substances. Their co-occurrence and metabolic features suggest that Helarchaeota may metabolize synergistically with some SRB, and together exert an important influence on the carbon cycle by mitigating the hydrocarbon emission from sediments to the overlying ocean. ISME Communications (2021) 1:25 ; https://doi.org/10.1038/s43705-021-00027-x INTRODUCTION lineages, such as Helarchaeota [19] in hydrothermal sediments in Many of the total microbial cells in the marine environment are the Guaymas Basin (GB) and Sifarchaetoa in organic-rich estimated to be present in marine sediments [1], of which a sediments of the Costa Rica Margin [20]. considerable fraction are archaea [2–4]. Although archaeal commu- Genome analysis and laboratory cultures suggest that some nities in oligotrophic and often oxic sediments are dominated by Asgard archaea in marine sediments will need external partner aerobic ammonia-oxidizing Thaumarchaeota [5–8], those in coastal cells to consume the reducing equivalents (e.g., in the forms of and often organic-rich sediments are more diverse and complex [9], hydrogen and formate) generated during organic matter degra- and their metabolic activity exerts a critical influence on the carbon dation [18, 21]. Helarchaeota from GB encode the Methyl-CoM and nutrient cycling on the global scale (e.g., [10–12]). reductase-like complex (MCR-like complex) and are proposed The Asgard superphylum of archaea is of evolutionary to be capable of oxidizing short-chain alkanes to conserve importance because its present-day members are thought to energy [19], using a pathway similar as other thermophilic share a common ancestor with modern eukaryotes [13, 14]. The alkane-oxidizing Euryarchaeota enriched from the same location archaeal phyla of this superphylum, including but not limited to [22, 23]. Most of these characterized alkane-oxidizing archaea form Lokiarchaeota, Thorarchaeota, Odinarchaeota, and Heimdallarch- consortia with sulfate-reducing bacteria (SRB) that use the aeota, have been established by metagenome-assembled gen- reducing equivalents released during alkane oxidation for sulfate omes (e.g., [13, 15]). A recent analysis of available Asgard 16S rRNA reduction [22–24], although some alkane-oxidizing archaea can gene sequences [16] showed that some sequences cannot be also channel the electrons to their own internal methanogenesis resolved to the existing lineages and thus suggested the diversity pathway [24, 25]. As a prevalent SRB in hydrothermal sediments, of Asgard archaea is likely broader than currently recognized [17]. Candidatus Desulfofervidus auxilii [26] is the dominant partner Marine sediment is the natural habitat of the only cultured Asgard bacteria of the characterized alkane-oxidizing Euryarchaeota in archaeon Candidatus Prometheoarchaeum syntrophicum MK-D1 heated marine sediments [22, 23]. However, the potential sinks of [18] and the vast majority of known Asgard archaea discovered via the reducing equivalents of Helarchaeota in other sediment metagenomic analysis [13, 14], so further exploration of marine environments remain elusive. sediment is promising to increase our understanding about this Scientific drilling off the Costa Rica Margin during International fascinating branch of life by recovering more novel lineages. This Ocean Drilling Program (IODP) Expedition 334 provided an speculation is supported by the recent discovery of new Asgard excellent avenue to explore the diversity of archaea, because ✉ 1School of Marine Science and Policy, University of Delaware, Lewes, DE, USA. email: [email protected] Received: 19 January 2021 Revised: 11 May 2021 Accepted: 26 May 2021 R. Zhao and J.F. Biddle 2 Fig. 1 Porewater profiles and microbial abundances in the sediments at IODP Site 1379 on the Costa Rica margin. Porewater profiles in meters below seafloor (meters bsf) were compiled from previous reports/publications of IODP Expedition 334 [30, 52]. Porewater profiles of sulfate (A), dissolved manganese (B), ammonium (C), and alkalinity (D) in the upper 10 m sediments in Hole U1379. E Abundances of archaeal and bacterial 16S rRNA genes quantified using qPCR with domain-specific primers. Stars denote the four sediment horizons where metagenome sequencing data was generated for this study. sediments from this location were shown to harbor high Microbial abundances and overall community structures abundances [27] and also phylogenetically novel lineages of We used domain-specific primers [6] to quantify the abundance of archaea [20, 28]. The drilled sites are in the forearc basin of the archaeal and bacterial 16S rRNA genes in the nine sediment subduction zone, where a considerable fraction of carbon horizons from 2 to 9 mbsf of Hole U1379B. Both archaeal and exchange between Earth’s surface and interior occurs [29]. bacterial 16S rRNA gene abundances are stable throughout the Abundant thermogenic alkanes (ethane, propane, and butane) examined sediments (Fig. 1E). However, archaea are about one were detected in the deep sediments, but not the surface order of magnitude lower than bacteria, resulting in bacterial sediments [30, 31]. This prompted us to perform further dominance in most of the studied samples except the shallowest 1234567890();,: metagenomic sequencing and analysis on shallow sediment sample (~2 mbsf). samples from this expedition, to explore the mechanisms of In order to maximize archaeal genome recovery, we selected four alkane depletion in this unique setting. Here, we report three new sediment horizons (2.45, 3.20, 7.70, and 8.23 mbsf) for shotgun Helarchaeota metagenome-assembled genomes (MAGs) in shal- metagenome sequencing, due to the high proportions of archaea in low sediments of Hole U1379B, each of which has three variants of these sediment horizons assessed by qPCR (Fig. 1E). We examined the MCR-like complex and could be significant alkane-oxidizing the microbial community structures in these four samples by 16S archaea in this sediment. These Helarchaeota account for the rRNA gene analyses based on both the un-assembled metagenome majority of the mcrA-bearing archaea community, with the rest of reads and the 16S rRNA gene amplicon sequencing data (Fig. 2). mcrA-bearing archaea affiliated to the typically methanotrophic Based on the metagenome data, in the archaeal domain, Bath- family of ANME-1. We also recovered five novel MAGs of sulfate- yarchaeota is the major archaeal phylum and accounts for on reducing bacteria in the class of Desulfobacteria, some of which average 44.7% (37.7–51.2% in individual samples) of the total could be the syntrophic partners of Helarchaeota due to their co- communities, while Asgard archaea especially Lokiarchaeota were occurring pattern and their matched metabolic capacities of H2 also detected to account for on average 5.6% (2.6–8.7% in individual and formate utilization. This study expands our understanding samples) of the total communities (Fig. 2a). In the bacterial domain, about the diversity, metabolic functions, and interspecies depen- Chloroflexi is the most dominant phylum, which accounts for on dency of Helarchaeota, which could exert a profound influence on average 19.0% of the total communities in different depths. Other the volatile carbon exchange between marine sediments and the major bacterial phyla include Acidobacteria, Actinobacteria, Elusi- overlying seawater. microbia, Planctomycetes, and Proteobacteria (mainly Deltaproteo- bacteria) (Fig. 2A). Similar results were also obtained from the 16S rRNA gene amplicon sequencing and analysis (Fig. 2B). These results RESULTS AND DISCUSSION are consistent with the previous assessments of microbial commu- Geochemical context nity structures of marine sediments off Costa Rica [27, 28]. IODP Site U1379 is located on the upper slope of the erosive subduction zone off the Osa Peninsula, Costa Rica. The sediment The presence and diversity of mcrA-bearing microbes pile at this site is estimated to be 890 m thick and is characterized As common
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