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Deep-sea methane seeps host highly diverse microbial communities whose biological diversity is distinct from other marine habitats. Coupled with microbial community analysis, untargeted metabolomics of environmental samples using high resolution tandem mass spectrometry provides unprecedented access to the unique specialized metabolisms of these chemosynthetic microorganisms. In addition, the diverse microbial natural products are of broad interest due to their potential applications for human and environmental health and well-being. In this exploratory study, sediment cores were collected from two methane seeps (-1000 m water depth) with very different gross geomorphologies, as well as a non-seep control site. Cores were subjected to parallel metabolomic and microbial community analyses to assess the feasibility of representative metabolite detection and identify congruent patterns between metabolites and microbes. Metabolomes generated using high resolution liquid chromatography tandem mass spectrometry were annotated with predicted structure classifications of the majority of mass features using SIRIUS and CANOPUS. The microbiome was characterized by analysis of 16S rRNA genes and analyzed both at the whole community level, as well as the small subgroup of Actinobacteria, which are known to produce societally useful compounds. Overall, the younger Dagorlad seep possessed a greater abundance of metabolites while there was more variation in abundance, number, and distribution of metabolites between samples at the older Emyn Muil seep. Lipid and lipid-like molecules displayed the greatest variation between sites and accounted for a larger proportion of metabolites found at the older seep. Overall, significant differences in composition of the microbial community mirrored the patterns of metabolite diversity within the samples; both varied greatly as a function of distance from methane seep, indicating a deterministic role of seepage. Interdisciplinary research to understand microbial and metabolic diversity is essential for understanding the processes and role of ubiquitous methane seeps in global systems and here we increase understanding of these systems by visualizing some of the chemical diversity that seeps add to marine systems. 

This work significantly advances our understanding of biodiversity and microbial interactions in herptile microbiomes, the role that fungi play as a structural and functional members of herptile gut microbiomes, and the chemical functions that structure microbiome phenotypes. We also provide an important observational system of how the gut microbiome represents a unique environment that selects for novel metabolic functions through horizontal gene transfer between fungi and bacteria. Such studies are needed to better understand the complexity of gut microbiomes in nature and will inform conservation strategies for threatened species of herpetofauna. 

Methane seeps are highly abundant marine habitats that contribute sources of chemosynthetic primary production to marine ecosystems. Seeps also factor into the global budget of methane, a potent greenhouse gas. Because of these factors, methane seeps influence not only local ocean ecology, but also biogeochemical cycles on a greater scale. Methane seeps host specialized microbial communities that vary significantly based on geography, seep gross morphology, biogeochemistry, and a diversity of other ecological factors including cross-domain species interactions. In this study, we collected sediment cores from six seep and non-seep locations from Grays and Quinault Canyons (46–47°N) off Washington State, USA, as well as one non-seep site off the coast of Oregon, USA (45°N) to quantify the scale of seep influence on biodiversity within marine habitats. These samples were profiled using 16S rRNA gene sequencing. Predicted gene functions were generated using the program PICRUSt2, and the community composition and predicted functions were compared among samples. The microbial communities at seeps varied by seep morphology and habitat, whereas the microbial communities at non-seep sites varied by water depth. Microbial community composition and predicted gene function clearly transitioned from on-seep to off-seep in samples collected from transects moving away from seeps, with a clear ecotone and high diversity where methane-fueled habitats transition into the non-seep deep sea. Our work demonstrates the microbial and metabolic sphere of influence that extends outwards from methane seep habitats. 

Abstract microbeMASST, a taxonomically informed mass spectrometry (MS) search tool, tackles limited microbial metabolite annotation in untargeted metabolomics experiments. Leveraging a curated database of >60,000 microbial monocultures, users can search known and unknown MS/MS spectra and link them to their respective microbial producers via MS/MS fragmentation patterns. Identification of microbe-derived metabolites and relative producers without a priori knowledge will vastly enhance the understanding of microorganisms’ role in ecology and human health.