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Desulfovibrio Diazotrophica Sp. Nov., a Sulphate Reducing Bacterium From bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.183566; this version posted July 2, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 1 Desulfovibrio diazotrophica sp. nov., a sulphate reducing bacterium from 2 the human gut capable of nitrogen fixation 3 4 Lizbeth Sayavedra1,2,#, Tianqi Li1,2,3, Marcelo Bueno Batista4, Brandon K.B. Seah5, Catherine 5 Booth1, Qixiao Zhai3, Wei Chen3, Arjan Narbad1,2 6 1Gut Health and Microbes, Quadram Institute Bioscience, Norwich Research Park, Norwich, 7 United Kingdom 8 2UK-China Joint Centre on Probiotic Bacteria, Norwich, United Kingdom and Wuxi, China 9 3State Key Laboratory of Food Science and Technology, School of Food Science and 10 Technology, Jiangnan University, Wuxi, China 11 4 Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, 12 Norwich, United Kingdom 13 5Max Planck Institute for Developmental Biology, Tübingen, Germany 14 15 #Address correspondence to Lizbeth Sayavedra, [email protected] 16 17 Running Head: D. diazotrophica can fix nitrogen 18 Keywords 19 Sulfate reduction; diazotroph; human gut microbiome 20 21 Abstract word count: 164 + 104 22 Text word count, not including Materials and Methods: 4,990 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.183566; this version posted July 2, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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 4.0 International license. 23 Abbreviations 24 ANI, average nucleotide identity; FAME, fatty acid methyl ester; D., Desulfovibrio; SRB, 25 sulphate reducing bacteria; TEM, transmission electron microscopy; SEM, scanning electron 26 microscopy; MAGs, metagenome-assembled genomes; WGS, whole genome sequencing; 27 T4SS, type IV secretion system; MCP, methyl-accepting chemotaxis protein 28 Abstract 29 Sulphate-reducing bacteria (SRB) are widespread in human guts, yet their expansion has been 30 linked to colonic diseases. We report the isolation, genome sequencing, and physiological 31 characterisation of a novel SRB species belonging to the class Deltaproteobacteria 32 (QI0027T). Phylogenomic analysis revealed that the QI0027T strain belongs to the genus 33 Desulfovibrio with its closest relative being Desulfovibrio legallii. Metagenomic sequencing 34 of stool samples from 45 individuals, as well as comparison with 1690 Desulfovibrionaceae 35 metagenome-assembled genomes, revealed the presence of QI0027T in at least 22 further 36 individuals. QI0027T encoded nitrogen fixation genes and based on the acetylene reduction 37 assay, actively fixed nitrogen. Transcriptomics revealed that QI0027T overexpressed 45 genes 38 in nitrogen limiting conditions as compared to cultures supplemented with ammonia, 39 including nitrogenases, an urea uptake system and the urease enzyme complex. To the best of 40 our knowledge, this is the first Desulfovibrio human isolate for which nitrogen fixation has 41 been demonstrated. This isolate was named Desulfovibrio diazotrophica sp. nov., referring to 42 its ability to fix nitrogen (‘diazotroph’). 43 Importance 44 Animals are often nitrogen limited and have evolved diverse strategies to capture biologically 45 active nitrogen. These strategies range from amino acid transporters to stable associations 46 with beneficial microbes that can provide fixed nitrogen. Although frequently thought as a 47 nutrient-rich environment, nitrogen fixation can occur in the human gut of some populations, 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.183566; this version posted July 2, 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 4.0 International license. 48 but so far it has been attributed mainly to Clostridia and Klebsiella based on sequencing. We 49 have cultivated a novel Desulfovibrio from human gut origin which encoded, expressed and 50 actively used nitrogen fixation genes, suggesting that some sulphate reducing bacteria could 51 also play a role in the availability of nitrogen in the gut. 52 Full text 53 Introduction 54 Sulphate reducing bacteria (SRB) are present in the mouth and the gut of ~50% of the human 55 population (1, 2). SRB thrive in the gut, releasing hydrogen sulphide (H2S) as a by-product of 56 sulphate reduction. H2S is a potent genotoxin and has been linked to chronic colonic 57 disorders and inflammation of the large intestine (3). Likewise, the presence of some 58 Desulfovibrio species has been implicated in chronic periodontitis, cell death and 59 inflammatory bowel diseases such as ulcerative colitis and Crohn’s disease (4). The 60 detrimental role of SRB is, however, not firmly established. H2S can also act as a signalling 61 molecule or energy source for mitochondria (5, 6). Moreover, by using hydrogen, SRB help 62 in the efficient energy acquisition and complete oxidation of substrates produced by 63 fermentative bacteria (7). SRB could, therefore, have a dual role in the gut microbiome. 64 Relatively few strains from healthy host individuals have been characterized. Cultivated SRB 65 isolated from humans include Desulfovibrio piger, D. fairfieldensis, D. desulfuricans and D. 66 legallii (4, 8), with D. piger described as the most abundant in samples obtained from western 67 countries (9). The physiology and genomic potential of strains isolated from non-western 68 countries remain largely unexplored. 69 Biological nitrogen fixation is the process by which gaseous dinitrogen (N2) is reduced to 70 biologically available ammonia (NH3) by diazotrophic microbes (10). Diazotrophy was 71 reported in some Desulfovibrio species from free-living communities and the termite gut (11, 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.183566; this version posted July 2, 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 4.0 International license. 72 12). All animals require access to a source of fixed nitrogen (13). Most of the readily 73 available nitrogen in humans comes from food, but nitrogen fixation can occur in the 74 microbiome of some human populations (14). In the human microbiome, the potential to fix 75 nitrogen has been so far linked to Klebsiella and Clostridia (14). The human host can regulate 76 the nitrogen available to the microbiome through the diet and intestinal secretions (15), so 77 bacteria that can fix nitrogen could potentially have a competitive advantage in the gut 78 environment. 79 We report here the isolation and characterization of a novel species of the genus 80 Desulfovibrio, strain QI0027T, isolated from a stool sample provided by a Chinese male 81 donor. Surprisingly this strain encoded the genes for nitrogen fixation. The goals of this study 82 were (i) to characterize strain QI0027T, (ii) to identify if diazotrophy is commonly distributed 83 among Desulfovibrionaceae associated to humans and (iii) to examine if the genes required 84 for nitrogen fixation are expressed and functional. We used metagenomic sequencing of 45 85 human donors, as well as analysed comprehensive collections of genomes recovered from 86 metagenomes to examine its distribution. We used physiological tests to examine the 87 nitrogenase activity. Finally, we used transcriptomics to determine the genes that are 88 expressed by QI0027T in response to the absence of a source of fixed nitrogen. 89 Results 90 Genome sequencing and phylogenomics 91 As part of a study to isolate and characterize SRB from Chinese donors, we isolated strain 92 QI0027T. Sequencing of QI0027T resulted in a 2.85 Mb genome, which was 99.1% complete 93 based on conserved Deltaproteobacteria marker genes and had a 62.1% GC content (Table 94 1). Comparison of the 16S rRNA from QI0027T against the SILVA SSU r138 database 95 revealed that the isolate belongs to the Deltaproteobacteria class and that its closest relative 96 is Desulfovibrio legallii. Even though the 16S rRNA gene of QI0027T shared a 99% identity 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.01.183566; this version posted July 2, 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 4.0 International license. 97 with the partial 16S rRNA sequence of D. legallii, the average nucleotide identity (ANI) of 98 their whole genomes was only 86.49%, which was well below the recommended threshold 99 for species discrimination of 94-96% ANI (16). Thus, QI0027T and D. legallii are different 100 species. 101 Consistent with our 16S rRNA comparison, the closest relative of QI0027T was D. legallii, 102 and these bacteria grouped within the ‘sensu-stricto’ Desulfovibrio based on a well-supported 103 phylogenomic tree reconstructed using 30 marker genes (17) (Figure 1). The family 104 Desulfovibrionaceae has eight described genera: Desulfovibrio, Bilophila, Lawsonia, 105 Halodesulfovibrio, Pseudodesulfovibrio, Desulfocurvus, and Desulfobaculum, although no 106 representative genomes have been sequenced for the former two genera. Bacteria from the 107 genera Maihella, Bilophila and Lawsonia grouped closer to the ‘sensu-stricto’ Desulfovibrio 108 as compared to Halodesulfovibrio, Pseudodesulfovibrio, and other Desulfovibrio bacteria that 109 despite their names, are different genera from the Desulfovibrionaceae family (Figure 1) (18). 110 Physiology 111 Similar to other Desulfovibrionaceae bacteria, QIOO27T is a gram-negative bacterium with 112 curved-rod to spirochete shape (Figure 2). Cells were 1.4 to 5 μm long. QI0027T grew at a 113 temperature between 15 to 46°C, with optimum growth temperature of 37°C.
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