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Genome Diversification in Globally Distributed Novel Marine bioRxiv preprint doi: https://doi.org/10.1101/814418; this version posted October 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Genome diversification in globally distributed novel 2 marine Proteobacteria is linked to environmental adaptation 3 4 Authors: Zhichao Zhou1, Patricia Q. Tran1, 2, Kristopher Kieft1, Karthik Anantharaman1* 5 6 7 Affiliations: 8 1Department of Bacteriology, University of Wisconsin–Madison, Madison, WI, 53706, USA 9 2Department of Integrative Biology, University of Wisconsin–Madison, Madison, WI 53706, 10 USA 11 12 13 *Corresponding author 14 Email: [email protected] 15 Address: 4550 Microbial Sciences Building, 1550 Linden Dr., Madison, WI, 53706 16 17 Abstract 18 Proteobacteria constitute the most diverse and abundant group of microbes on Earth. In 19 productive marine environments like deep-sea hydrothermal systems, Proteobacteria have been 20 implicated in autotrophy coupled to sulfur, methane, and hydrogen oxidation, sulfate reduction, 21 and denitrification. Beyond chemoautotrophy, little is known about the ecological significance 22 of novel Proteobacteria that are globally distributed and active in hydrothermal systems. Here 23 we apply multi-omics to characterize 51 metagenome-assembled genomes from three 24 hydrothermal vent plumes in the Pacific and Atlantic Oceans that are affiliated with nine novel 25 Proteobacteria lineages. Metabolic analyses revealed these organisms to contain a diverse 26 functional repertoire including chemolithotrophic ability to utilize sulfur and C1 compounds, 27 and chemoorganotrophic ability to utilize environment-derived fatty acids, aromatics, 28 carbohydrates, and peptides. Comparative genomics with marine and terrestrial microbiomes 29 suggests that lineage-associated functional traits could explain niche specificity. Our results 30 shed light on the ecological functions and metabolic strategies of novel Proteobacteria in 31 hydrothermal systems and beyond, and highlight the relationship between genome 32 diversification and environmental adaptation. 33 34 Introduction 35 Proteobacteria constitute one of the most diverse microbial phyla and are successful in most 36 biomes on Earth. Proteobacteria are abundant from pole to pole in the world’s oceans1, 2, and 37 also from the surface to the deep oceans in vertical cross-sections3, 4. Unlike other microbial 38 lineages, Proteobacteria display an enormous functional repertoire and comprise phototrophs, 39 autotrophs, and heterotrophs. In the surface oceans, heterotrophic proteobacteria such as 1 bioRxiv preprint doi: https://doi.org/10.1101/814418; this version posted October 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 40 SAR11, SAR86, and Roseobacter are abundant and highly successful bacterioplankton lineages 41 which mainly rely on the availability and distribution of dissolved organic matter5. 42 Phototrophic proteobacteria include groups of Alphaproteobacteria and Gammaproteobacteria 43 that together comprise the group referred to as ‘marine aerobic anoxygenic phototrophs’ 44 (AAnPs) that are capable of bacteriochlorophyll-dependent photosynthesis and can influence 45 overall carbon and energy budgets in the oceans6. In the dark oceans, Proteobacteria drive 46 carbon cycling through primary production associated with sulfur and methane oxidation7, as 47 well as heterotrophy8. Given their abundance across marine environments and their wide range 48 of metabolic traits, Proteobacteria represent an ideal lineage to investigate links between 49 genome diversification and environmental adaptation. To constrain the environment in which 50 to explore this question, we studied the distribution, metabolism, activity, and ecology of 51 proteobacteria in deep-sea hydrothermal plumes, a system characterized by the presence of 52 natural geochemical gradients. 53 54 Hydrothermal plumes are formed when hot fluids (up to 400°C) emanate from deep-sea 55 hydrothermal vents and mix with cold deep ocean waters (2-4°C). This process causes steep 56 thermal and chemical gradients at small spatial scales, and biotic and abiotic processes leading 57 to the formation of a variety of ecological niches that can be exploited by microorganisms9, 10, 58 11. Hydrothermal fluids typically entrain substantial concentrations of reduced chemicals and 59 substrates, e.g., hydrogen (H2), methane (CH4), hydrogen sulfide (H2S), ammonia (NH3), 60 methanol, C1 compounds (formaldehyde, formate, and carbon monoxide), hydrocarbons and 61 metals (Fe, Mn, As, and etc) 12 13, 14, 15, 16, 17, 18, 19, 20. Hydrothermal biogeochemistry strongly 62 influences microbial community composition in the plume and surrounding environments10. In 63 chemosynthetic environments of the oceans such as hydrothermal systems, proteobacterial 64 groups actively participate in primary production by utilizing a wide variety of reduced 65 substrates10, 21. Specific examples include diverse and active populations of Sulfurimonas and 66 Sulfurovum (Epsilonproteobacteria) species that oxidize reduced sulfur compounds; 67 Thioglobus/SUP05 and Beggiatoa (Gammaproteobacteria) that oxidize reduced sulfur 68 compounds and hydrogen for energy generation10; and Methylophaga and Methylococcaceae 69 (Gammaproteobacteria) that can oxidize methane, methanol, and hydrocarbons22. 70 71 Besides plumes, hydrothermal systems host several chemosynthetic environments dominated 72 by Proteobacteria. Thermophilic Epsilonproteobacteria belonging to the genera Nautilia and 73 Lebetimonas that can oxidize hydrogen with elemental sulfur, are prevalent on the 74 hydrothermal vent deposits23. On the periphery of the venting area with lower temperatures (< 75 55°C), vent animals (such as tubeworms, crabs, bivalves) depend on the chemosynthetic 76 symbiotic Proteobacteria as the source of organic carbon and energy10. Typically, 77 proteobacterial endosymbionts (mostly Gammaproteobacteria) of tubeworms can oxidize 78 reduced sulfur species24, while proteobacterial endosymbionts of bivalves can perform 79 oxidation of reduced sulfur, methane, hydrogen and carbon monoxide24, 25, 26. Beyond these 80 host animals, little is known about whether other microbes could also utilize organic 81 compounds from vent-derived chemosynthesis9. Organic carbon from primary production may 2 bioRxiv preprint doi: https://doi.org/10.1101/814418; this version posted October 22, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 82 be used in heterotrophy in hydrothermal plumes as they disperse or even be consumed locally 83 in vent-associated environments. However, due to the predisposition of hydrothermal plumes 84 as chemosynthetic environments, microorganisms especially bacteria associated with 85 heterotrophy in plumes remain little-studied. Organisms in deep-sea systems are often versatile 86 and can exhibit mixotrophic characteristics. To elucidate the versatile metabolism, evolutionary 87 relationships, and ecology of abundant groups of little-characterized deep-sea Proteobacteria, 88 we reconstructed and compared genomes, transcriptomes, and protein families to 89 Proteobacteria from other terrestrial and marine biomes. 90 91 In this study, we reconstructed 51 novel proteobacterial genomes from the deep-sea 92 hydrothermal plumes and surrounding background seawaters at three distinct locations, namely 93 Guaymas Basin and Lau Basin in the Pacific Ocean, and Mid-Cayman Rise in the Atlantic 94 Ocean. These hydrothermal systems comprise gradients in ocean depth (~1900m to 5000m), 95 geophysical parameters (back-arc basin to sedimented hydrothermal system), and chemistry27, 96 28, 29. Our genome-resolved metagenomics approach has allowed the discovery of novel 97 microbial groups of Proteobacteria based on phylogeny reconstructed using both concatenated 98 ribosomal proteins and 16S rRNA genes and identified metabolic characteristics of specific 99 proteobacterial organisms and lineages. Metatranscriptomics-derived measurements enabled 100 us to describe and compare the activity of novel Proteobacteria across a range of environments 101 within and between different plumes and deep ocean samples. The ecological and functional 102 knowledge associated with the metabolism of these novel microbial groups provides insights 103 into organic carbon metabolism, energy transformations, and adaptive strategies in 104 hydrothermal vent ecosystems and beyond. While primarily found in hydrothermal systems, 105 these novel Proteobacteria have a worldwide distribution and can be observed outside of marine 106 environments including freshwaters and the terrestrial subsurface. Overall, our study reveals 107 that genome diversification in globally prevalent and abundant Proteobacteria is associated 108 with environmental adaptation and suggests that the distribution of functional traits could 109 potentially explain their niche-adapting mechanisms. 110 111 Results 112 Sampling and reconstruction of genomes from deep-sea hydrothermal
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