Horizontal Acquisition of a Patchwork Calvin Cycle by Symbiotic and Free-Living Campylobacterota (Formerly Epsilonproteobacteria)

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Horizontal Acquisition of a Patchwork Calvin Cycle by Symbiotic and Free-Living Campylobacterota (Formerly Epsilonproteobacteria) The ISME Journal (2020) 14:104–122 https://doi.org/10.1038/s41396-019-0508-7 ARTICLE Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria) 1,9 1 1,10 1 1,2 Adrien Assié ● Nikolaus Leisch ● Dimitri V. Meier ● Harald Gruber-Vodicka ● Halina E. Tegetmeyer ● 1 3,4 3,5,6 7 7,11 Anke Meyerdierks ● Manuel Kleiner ● Tjorven Hinzke ● Samantha Joye ● Matthew Saxton ● 1,8 1,10 Nicole Dubilier ● Jillian M. Petersen Received: 7 April 2019 / Revised: 6 August 2019 / Accepted: 15 August 2019 / Published online: 27 September 2019 © The Author(s) 2019. This article is published with open access Abstract Most autotrophs use the Calvin–Benson–Bassham (CBB) cycle for carbon fixation. In contrast, all currently described autotrophs from the Campylobacterota (previously Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We discovered campylobacterotal epibionts (“Candidatus Thiobarba”) of deep-sea mussels that have acquired a complete CBB cycle and may have lost most key genes of the rTCA cycle. Intriguingly, the phylogenies of campylobacterotal CBB cycle genes suggest they were acquired in multiple transfers from Gammaproteobacteria closely 1234567890();,: 1234567890();,: related to sulfur-oxidizing endosymbionts associated with the mussels, as well as from Betaproteobacteria. We hypothesize that “Ca. Thiobarba” switched from the rTCA cycle to a fully functional CBB cycle during its evolution, by acquiring genes from multiple sources, including co-occurring symbionts. We also found key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be more widespread in this phylum than previously known. Metatranscriptomics and metaproteomics confirmed high expression of CBB cycle genes in mussel-associated “Ca. Thiobarba”. Direct stable isotope fingerprinting showed that “Ca. Thiobarba” has typical CBB signatures, suggesting that it uses this cycle for carbon fixation. Our discovery calls into question current assumptions about the distribution of carbon fixation pathways in microbial lineages, and the interpretation of stable isotope measurements in the environment. Introduction These authors contributed equally: Adrien Assié, Nikolaus Leisch All life on Earth is based on carbon fixation, and its Supplementary information The online version of this article (https:// molecular machinery is increasingly becoming a focus of doi.org/10.1038/s41396-019-0508-7) contains supplementary biotechnology and geo-engineering efforts due to its material, which is available to authorized users. * Adrien Assié 5 Department of Pharmaceutical Biotechnology, University of [email protected] Greifswald, Institute of Pharmacy, D-17489 Greifswald, Germany * Nicole Dubilier 6 [email protected] Institute of Marine Biotechnology, D-17489 Greifswald, Germany 7 * Jillian M. Petersen Department of Marine Sciences, The University of Georgia, Room [email protected] 159, Marine Sciences Bldg, Athens, GA 30602-3636, USA 8 MARUM—Zentrum für Marine Umweltwissenschaften, 1 Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, University of Bremen, Leobener Str. 2, 28359 Bremen, Germany D-28359 Bremen, Germany 9 Present address: Baylor College of Medicine, One Baylor Plaza, 2 Center for Biotechnology, Bielefeld University, Houston, TX 77030, USA Universitaetsstrasse 27, 33615 Bielefeld, Germany 10 Present address: Centre for Microbiology and Environmental 3 Department of Geoscience, University of Calgary, 2500 University Systems Science, Division of Microbial Ecology, University of Drive Northwest, Alberta, Calgary, AB T2N 1N4, Canada Vienna, Althanstrasse 14, 1090 Vienna, Austria 11 4 Department of Plant and Microbial Biology, North Carolina State Present address: Department of Biological Sciences, Miami University, Raleigh, NC 27695, USA University, 4200N University Blvd, Middletown, OH 45042, USA Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota. 105 potential to improve crop yields and sequester carbon endosymbionts, which they rely on for most of their nutri- dioxide from the atmosphere [1]. Seven carbon fixation tion [27, 28]. Some vent and seep invertebrates associate pathways have evolved in nature, and one purely synthetic with both gammaproteobacterial and campylobacterotal pathwayrunsinvitro[2–4]. Of the seven natural path- symbionts simultaneously, which raises the question of how ways, the Calvin–Benson–Bassham (CBB) cycle was the these co-occurring symbionts with differing habitat pre- first discovered, and is believed to be the most widespread ferences can both be provided with suitable conditions [5–7]. The CBB cycle is used by a diverse array of [27, 29, 30]. organisms throughout the tree of life, including plants and Bathymodiolin mussels, a subfamily of mytilid bivalves, algae, cyanobacteria, and autotrophic members of the are found worldwide at hydrothermal vents and cold seeps Alpha-, Beta-, and Gammaproteobacteria. Its key enzyme, [31]. They have evolved symbiotic relationships with che- the ribulose 1,5-bisphosphate carboxylase/oxygenase mosynthetic bacteria, allowing them to colonize these (RuBisCO) is thought to be the most abundant, as well as extreme environments. Inside their gills, they host intra- one of the most ancient enzymes on Earth [8, 9]. cellular gammaproteobacterial endosymbionts in epithelial The reductive tricarboxylic acid (rTCA) cycle was the cells called bacteriocytes. The dominant endosymbionts are second described carbon fixation pathway [10]. In short, it sulfur- and methane-oxidizing bacteria, often co-occurring is a reversal of the energy-generating oxidative TCA cycle. in the same mussel species. Some sulfur-oxidizing sym- Instead of oxidizing acetyl-CoA and generating ATP and bionts also use hydrogen as an energy source, and some reducing equivalents, it reduces CO2 at the expense of ATP mussel species host additional symbionts that gain energy and reducing equivalents [2, 7, 10]. Most of the enzymes from short-chain alkanes [32, 33]. In addition to these are shared with the TCA cycle, except for those that cata- dominant endosymbionts, Assié et al. recently discovered lyze irreversible reactions in the TCA, such as citrate syn- epibionts that colonize bathymodiolin mussels from around thase, which is catalyzed by ATP citrate lyase in the the world [34]. In contrast to the gammaproteobacterial rTCA cycle. However, given sufficiently high reactant to endosymbionts of bathymodiolins, these epibionts belong to product ratios and enzyme concentrations, the citrate syn- the Campylobacterota. They are filamentous and colonize thase reaction can be reversed to run the TCA cycle the surfaces of the gill epithelia in dense patches in the reductively, without any additional enzymes [11, 12]. The extracellular spaces between the gill filaments, through rTCA pathway is widely distributed in nature, and has which the mussel pumps the inflow of oxygenated seawater been described in diverse lineages of anaerobes and (Fig. S1). The nature of the association between the epi- microaerobes, such as the Chlorobi, Aquificae, Nitrospirae, biotic Campylobacterota and their mussel hosts is not clear. and is also commonly observed among the Proteobacteria, Similar associations in other deep-sea invertebrates, such as including the Deltaproteobacteria and the Campylobacter- Kiwa crabs [35], gastropods [36], and shallow-water ota, (formerly Epsilonproteobacteria) [13, 14]. It is parti- nematodes [37] are thought to be beneficial or commensal. cularly prominent in the Campylobacterota, as all In this study, we used a multi-omics approach to inves- previously described autotrophic members of this class use tigate the metabolism of the Campylobacterota epibionts in the rTCA pathway for CO2 fixation [2, 13]. two bathymodiolin mussels species, “Bathymodiolus” Carbon fixation by chemoautotrophic microorganisms childressi from cold seeps in the Gulf of Mexico, which forms the basis of entire ecosystems at deep-sea hydro- have only methane oxidizers as their dominant endo- thermal vents and cold seeps [15, 16]. Most of this carbon is symbiont, and Bathymodiolus azoricus from the Mid- fixed either via the CBB cycle, used by many gammapro- Atlantic Ridge, which host both a sulfur- and a methane- teobacterial autotrophs, or the rTCA cycle, used by cam- oxidizing endosymbiont [27]. Unexpectedly, the epibionts pylobacterotal autotrophs. This difference is reflected by the had, and expressed, all genes required for the CBB cycle but different niches colonized by these organisms at hydro- appeared to lack key genes of the rTCA cycle. These CBB thermal vents and seeps, with Gammaproteobacteria typi- cycle genes were most likely acquired by horizontal gene cally dominating habitats with higher oxygen and lower transfer (HGT) from diverse sources. With a recently sulfide concentrations where the CBB cycle would be more developed, highly sensitive, direct stable isotope finger- efficient, and Campylobacterota typically thriving at lower printing technique [38], we show that the proteins of these oxygen and higher sulfide concentrations where the rTCA epibionts had an isotopic signature typical of the CBB cycle could provide a selective advantage [17–23]. cycle, further demonstrating its importance for the meta- Experimental studies have linked substrate preferences in bolism of these epibionts. The discovery of Campylo- cultured Gammaproteobacteria and Campylobacterota to bacterota that use
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