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Anaerobic Sulfur Oxidation Underlies Adaptation of a Chemosynthetic Symbiont To bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted March 18, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to 2 oxic-anoxic interfaces 3 4 Running title: chemosynthetic ectosymbiont’s response to oxygen 5 6 Gabriela F. Paredes1, Tobias Viehboeck1,2, Raymond Lee3, Marton Palatinszky2, Michaela A. 7 Mausz4, Sigfried Reipert5, Arno Schintlmeister2,6, Jean-Marie Volland1,‡, Claudia Hirschfeld7 8 Michael Wagner2,8, David Berry2,9, Stephanie Markert7, Silvia Bulgheresi1,* and Lena König1,* 9 10 1 University of Vienna, Department of Functional and Evolutionary Ecology, Environmental 11 Cell Biology Group, Vienna, Austria 12 13 2 University of Vienna, Center for Microbiology and Environmental Systems Science, Division 14 of Microbial Ecology, Vienna, Austria 15 16 3 Washington State University, School of Biological Sciences, Pullman, WA, USA 17 18 4 University of Warwick, School of Life Sciences, Coventry, UK 19 20 5 University of Vienna, Core Facility Cell Imaging and Ultrastructure Research, Vienna, 21 Austria 22 23 6 University of Vienna, Center for Microbiology and Environmental Systems Science, Large- 24 Instrument Facility for Environmental and Isotope Mass Spectrometry, Vienna, Austria 25 26 7 University of Greifswald, Institute of Pharmacy, Department of Pharmaceutical 27 Biotechnology, Greifswald, Germany 28 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted March 18, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 29 8 Aalborg University, Department of Chemistry and Bioscience, Aalborg, Denmark 30 9 Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna, 31 Vienna, Austria 32 33 ‡ Present affiliation: Joint Genome Institute/Global Viral, San Francisco, CA, USA 34 35 Corresponding Authors 36 37 Silvia Bulgheresi: University of Vienna, Department of Functional and Evolutionary Ecology, 38 Environmental Cell Biology Group, Althanstrasse 14, 1090 Vienna, Austria, +43-1-4277- 39 76514, [email protected] 40 41 Lena König: University of Vienna, Department of Functional and Evolutionary Ecology, 42 Environmental Cell Biology Group, Althanstrasse 14, 1090 Vienna, Austria, +43-1-4277- 43 76527, [email protected] 44 45 * These authors contributed equally to this work. 46 47 Competing Interests 48 The authors declare no competing financial interest. 49 50 51 52 53 54 55 56 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted March 18, 2020. 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. 57 Abstract 58 Chemosynthetic symbioses occur worldwide in marine habitats. However, physiological 59 studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are 60 coated by monocultures of thiotrophic Gammaproteobacteria. As these nematodes migrate 61 through the redox zone, their ectosymbionts experience varying oxygen concentrations. 62 Here, by applying omics, Raman microspectroscopy and stable isotope labeling, we 63 investigated the effect of oxygen on the metabolism of Candidatus Thiosymbion oneisti. 64 Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, 65 but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, 66 several genes involved in carbon fixation, the assimilation of organic carbon and 67 polyhydroxyalkanoate (PHA) biosynthesis, as well as nitrogen fixation and urea utilization 68 were upregulated in oxic conditions. Furthermore, in the presence of oxygen, stress-related 69 genes were upregulated together with vitamin and cofactor biosynthesis genes likely 70 necessary to withstand its deleterious effects. 71 Based on this first global physiological study of a chemosynthetic ectosymbiont, we 72 propose that, in anoxic sediment, it proliferates by utilizing nitrate to oxidize reduced sulfur, 73 whereas in superficial sediment it exploits aerobic respiration to facilitate assimilation of 74 carbon and nitrogen to survive oxidative stress. Both anaerobic sulfur oxidation and its 75 decoupling from carbon fixation represent unprecedented adaptations among 76 chemosynthetic symbionts. 77 78 Introduction 79 At least six animal phyla and numerous lineages of bacterial symbionts belonging to Alpha-, 80 Delta-, Gamma- and Epsilonproteobacteria engage in chemosynthetic symbioses, rendering 81 the evolutionary success of these associations incontestable [1, 2]. Many of these 82 mutualistic associations rely on sulfur-oxidizing (thiotrophic), chemoautotrophic bacterial 83 symbionts, that oxidize reduced sulfur compounds for energy generation in order to fix 84 inorganic carbon (CO2) for biomass build-up. Particularly in binary symbioses involving 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted March 18, 2020. 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. 85 intracorporeal thiotrophic bacteria, it is generally accepted that the endosymbiont’s 86 chemosynthetic metabolism serves to provide organic carbon for feeding the animal host 87 [reviewed in 1–3]. In addition, some chemosynthetic symbionts have been found capable to 88 fix atmospheric nitrogen, albeit symbiont-to-host transfer of fixed nitrogen remains unproven 89 [4, 5]. As for the rarer chemosynthetic bacterial-animal associations in which symbionts 90 colonize exterior surfaces (ectosymbionts), fixation of inorganic carbon and transfer of 91 organic carbon to the host has only been demonstrated for the microbial community 92 colonizing the gill chamber of the hydrothermal vent shrimp Rimicaris exoculata [6]. 93 In this study, we focused on Candidatus Thiosymbion oneisti, a 94 Gammaproteobacterium belonging to the basal family of Chromatiaceae (also known as 95 purple sulfur bacteria), which colonizes the surface of the marine nematode Laxus oneistus 96 (Stilbonematinae). Curiously, this group of free-living roundworms represents the only known 97 animals engaging in monospecific ectosymbioses, i.e. each nematode species is 98 ensheathed by a single Ca. Thiosymbion phylotype, and, in the case of Ca. T. oneisti, the 99 bacteria form a single layer on the cuticle of its host [7–11]. Moreover, the rod-shaped 100 representatives of this bacterial genus, including Ca. T. oneisti, divide by FtsZ-based 101 longitudinal fission, a unique reproductive strategy which ensures continuous and 102 transgenerational host-attachment [12–14]. 103 Like other chemosynthetic symbionts, Ca. Thiosymbion have been considered 104 chemoautotrophic sulfur oxidizers based on several lines of evidence: stable carbon isotope 105 ratios of symbiotic nematodes are comparable to those found in other chemosynthetic 106 symbioses [15]; the key enzyme for carbon fixation via the Calvin-Benson-Bassham cycle 107 (RuBisCO) along with enzymes involved in sulfur oxidation and elemental sulfur have been 108 detected [16–18]; reduced sulfur compounds (sulfide, thiosulfate) have been shown to be 109 taken up from the environment by the ectosymbionts, to be used as energy source, and to 110 be responsible for the white appearance of the symbiotic nematodes [18–20]; the animals 111 often occur in the sulfidic zone of marine shallow-water sands [21]. More recently, the 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted March 18, 2020. 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. 112 phylogenetic placement and genetic repertoire of Ca. Thiosymbion species have equally 113 been supporting the chemosynthetic nature of the symbiosis [5, 11]. 114 The majority of thioautotrophic symbioses have been described to rely on reduced 115 sulfur compounds as electron donors and oxygen as terminal electron acceptor [2, 3]. 116 However, given that sulfidic and oxic zones are often spatially separated, also owing to 117 abiotic sulfide oxidation [22, 23], chemosynthetic symbioses (1) are found where sulfide and 118 oxygen occur in close proximity (e.g., hydrothermal vents, shallow-water sediments) and (2) 119 host behavioral, physiological and anatomical adaptations are needed to enable thiotrophic 120 symbionts to access both substrates. Host-mediated migration across the substrate 121 gradients is perhaps the most commonly encountered behavioral adaptation and was 122 proposed for deep-sea crustaceans, as well as for shallow water interstitial invertebrates and 123 Kentrophoros ciliates [reviewed in 1, 2]. Also the symbionts of Stilbonematinae have long 124 been
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