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Anaerobic Sulfur Oxidation Underlies Adaptation of a Chemosynthetic Symbiont

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Anaerobic Sulfur Oxidation Underlies Adaptation of a Chemosynthetic Symbiont bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted January 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 2 to 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, 7 Michaela A. Mausz4, Siegfried Reipert5, Arno Schintlmeister2,6, Andreas Maier7, Jean- 8 Marie Volland1,*, Claudia Hirschfeld8, Michael Wagner2,9, David Berry2,10, Stephanie 9 Markert8, Silvia Bulgheresi1,# and Lena König1# 10 11 1 University of Vienna, Department of Functional and Evolutionary Ecology, 12 Environmental Cell Biology Group, Vienna, Austria 13 14 2 University of Vienna, Center for Microbiology and Environmental Systems Science, 15 Division of Microbial Ecology, Vienna, Austria 16 17 3 Washington State University, School of Biological Sciences, Pullman, WA, USA 18 19 4 University of Warwick, School of Life Sciences, Coventry, UK 20 21 5 University of Vienna, Core Facility Cell Imaging and Ultrastructure Research, Vienna, 22 Austria 23 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted January 28, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 24 6 University of Vienna, Center for Microbiology and Environmental Systems Science, 25 Large-Instrument Facility for Environmental and Isotope Mass Spectrometry, Vienna, 26 Austria 27 28 7 University of Vienna, Faculty of Geosciences, Geography, and Astronomy, Department 29 of Geography and Regional Research, Geoecology, Vienna, Austria 30 31 8 University of Greifswald, Institute of Pharmacy, Department of Pharmaceutical 32 Biotechnology, Greifswald, Germany 33 34 9 Aalborg University, Department of Chemistry and Bioscience, Aalborg, Denmark 35 36 10 Joint Microbiome Facility of the Medical University of Vienna and the University of 37 Vienna, Vienna, Austria 38 * Present affiliation: Joint Genome Institute/Global Viral, San Francisco, CA, USA 39 40 #Address correspondence to Silvia Bulgheresi, [email protected]. 41 #Address correspondence to Lena König, [email protected]. 42 43 Silvia Bulgheresi and Lena König contributed equally to this work. 44 45 46 47 48 49 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted January 28, 2021. 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. 50 ABSTRACT 51 Chemosynthetic symbioses occur worldwide in marine habitats, but 52 comprehensive physiological studies of chemoautotrophic bacteria thriving on animals 53 are scarce. Stilbonematinae are coated by monocultures of thiotrophic 54 Gammaproteobacteria. As these nematodes migrate through the redox zone, their 55 ectosymbionts experience varying oxygen concentrations. However, nothing is known 56 about how these variations affect their physiology or metabolism. Here, by applying 57 omics, Raman microspectroscopy and stable isotope labelling, we investigated the effect 58 of oxygen on Candidatus Thiosymbion oneisti. Unexpectedly, sulfur oxidation genes 59 were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and 60 incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in 61 carbon fixation were upregulated in oxic conditions, together with genes involved in 62 organic carbon assimilation, polyhydroxyalkanoate (PHA) biosynthesis, nitrogen fixation 63 and urea utilization. Furthermore, in the presence of oxygen, stress-related genes were 64 upregulated together with vitamin biosynthesis genes likely necessary to withstand its 65 deleterious effects, and the symbiont appeared to proliferate less. Based on its 66 physiological response to oxygen, we propose that Ca. T. oneisti may exploit anaerobic 67 sulfur oxidation coupled to denitrification to proliferate in anoxic sand. However, the 68 ectosymbiont would still profit from the oxygen available in superficial sand, as the 69 energy-efficient aerobic respiration would facilitate carbon and nitrogen assimilation by 70 the ectosymbiont. 71 72 IMPORTANCE Chemoautotrophic endosymbionts are famous for exploiting sulfur 73 oxidization to feed marine organisms with fixed carbon. However, the physiology of 74 thiotrophic bacteria thriving on the surface of animals (ectosymbionts) is less 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted January 28, 2021. 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. 75 understood. One long standing hypothesis posits that attachment to animals that migrate 76 between reduced and oxic environments would boost sulfur oxidation, as the 77 ectosymbionts would alternatively access sulfide and oxygen, the most favorable 78 electron acceptor. Here, we investigated the effect of oxygen on the physiology of 79 Candidatus Thiosymbion oneisti, a Gammaproteobacterium which lives attached to 80 marine nematodes inhabiting shallow water sand. Surprisingly, sulfur oxidation genes 81 were upregulated in anoxic relative to oxic conditions. Furthermore, under anoxia, the 82 ectosymbiont appeared to be less stressed and to proliferate more. We propose that 83 animal-mediated access to oxygen, rather than enhancing sulfur oxidation, would 84 facilitate assimilation of carbon and nitrogen by the ectosymbiont. 85 86 INTRODUCTION 87 At least six animal phyla and numerous lineages of bacterial symbionts belonging to 88 Alphaproteobacteria, Gammaproteobacteria, and Campylobacteria (formerly 89 Epsilonproteobacteria) (1) engage in chemosynthetic symbioses, rendering the 90 evolutionary success of these associations incontestable (2, 3). Many of these 91 mutualistic associations rely on sulfur-oxidizing (thiotrophic), chemoautotrophic bacterial 92 symbionts. These oxidize reduced sulfur compounds for energy generation in order to 93 fix inorganic carbon (CO2) for biomass build-up. Particularly in binary symbioses 94 involving thiotrophic endosymbionts, it is generally accepted that the bacterial 95 chemosynthetic metabolism serves to provide organic carbon for feeding the animal host 96 (reviewed in 2–4). In addition, some chemosynthetic symbionts have been found 97 capable to fix atmospheric nitrogen, albeit symbiont-to-host transfer of fixed nitrogen 98 remains unproven (5, 6). As for the rarer chemosynthetic bacterial-animal associations 99 in which symbionts colonize exterior surfaces (ectosymbioses), fixation of inorganic 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.03.17.994798; this version posted January 28, 2021. 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. 100 carbon and transfer of organic carbon to the host has only been unequivocally shown 101 for the microbial community colonizing the gill chamber of the hydrothermal vent shrimp 102 Rimicaris exoculata (7). 103 The majority of thioautotrophic symbioses have been described to rely on 104 reduced sulfur compounds as electron donors and oxygen as terminal electron acceptor 105 (3, 4). However, given that sulfidic and oxic zones are often spatially separated, also 106 owing to abiotic sulfide oxidation (8, 9), chemosynthetic symbioses (1) are typically found 107 where sulfide and oxygen occur in close proximity (e.g. hydrothermal vents, shallow- 108 water sediments) and/or (2) exhibit host behavioral, physiological and anatomical 109 adaptations enabling the symbionts to access both substrates. Among the former 110 adaptations, host-mediated migration across oxygen and sulfide gradients was 111 proposed for shallow water interstitial invertebrates and Kentrophoros ciliates (reviewed 112 in 2, 3). The symbionts of Stilbonematinae have also long been hypothesized to 113 associate with their motile nematode hosts to maximize sulfur oxidation-fueled 114 chemosynthesis, by alternatively accessing oxygen in upper sand layers and sulfide in 115 deeper, anoxic sand. This hypothesis was based upon the distribution pattern of 116 Stilbonematinae in sediment cores together with their migration patterns observed in 117 agar columns (10, 11, 12). However, several chemosynthetic symbionts were 118 subsequently shown to use nitrate as an alternative electron acceptor, and nitrate 119 respiration was stimulated by sulfide, suggesting that symbionts may gain energy by 120 respiring nitrate instead of oxygen (13-16). Furthermore, although physiological studies 121 on chemosynthetic symbioses are available (e.g. 17-19), the impact of oxygen on the 122 symbiont central metabolism has not been investigated (remarkably, not even in those 123 that
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