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Genome Sequencing and Functional Genes Comparison Between Sphingopyxis bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Genome sequencing and functional genes comparison between Sphingopyxis 2 USTB-05 and Sphingomonas morindae NBD5 3 4 Chao Liu1, Qianqian Xu1, Zhenzhen Zhao1, Shahbaz Ahmad1, Haiyang Zhang1, Yufan 5 Zhang1, Yu Pang1, Abudumukeyiti Aikemu1, Yang Liu1,* Hai Yan1,* 6 7 1 School of Chemistry and Biological Engineering, University of Science and 8 Technology Beijing, Beijing 100083, China 9 *Corresponding author: Prof Hai Yan; mail: [email protected]. Yang Liu; mail: 10 [email protected]. 11 12 Keywords: Sphingomonadaceae; Genome; Lutein; Hepatotoxin; Microcystins; 13 Biodegradation 14 15 16 17 18 19 20 21 22 23 24 25 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 26 ABSTRACT 27 Sphingomonadaceae has a large number of strains that can biodegrade hepatotoxins or 28 environmental pollutants. The latest research reported that certain strains can also 29 produce lutein. Based on the third-generation sequencing technology, we analyzed the 30 whole genome sequence and compared related functional genes of two strains of 31 Sphingomonadaceae isolated from different habitats. The genome of Sphingopyxis 32 USTB-05 was 4,679,489 bp and contained 4312 protein coding genes. The 4,239,716 33 bp nuclear genome of Sphingomonas morindae NBD5, harboring 3882 protein coding 34 genes, has two sets of chromosomes. Both strains had lutein synthesis metabolism 35 pathway sharing identical synthetic genes of crtB, crtE, crtI, crtQ, crtL, crtR, atoB, dxs, 36 dxr, ispD, ispE, ispDF, gcpE, ispG, ispH, ispA, ispB and ispU. Sphingopyxis USTB-05 37 had hepatotoxins microcystins and nodularin metabolic pathways related to 16 genes 38 (ald、ansA、gdhA、crnA、phy、ocd、hypdh、spuC、nspC、speE、murI、murD、 39 murC、hmgL、bioA and glsA), while these genes were not found in Sphingomonas 40 morindae NBD5. The unique protein sequences of strain NBD5 and strain USTB-05 41 were 155 and 199, respectively. The analysis of whole genome of the two 42 Sphingomonadaceae strains provides insights into prokaryote evolution, the new 43 pathway for lutein production and the new genes for environmental pollutant 44 biodegradation. 45 46 IMPORTANCE 47 Understanding the functional genes related to the special functions of strains is essential 48 for humans to utilize microbial resources. The ability of Sphingopyxis USTB-05 to 49 degrade hepatotoxins microcystins and nodularin has been studied in depth, however 50 the complete metabolic process still needs further elucidation. Sphingomonas morindae 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 51 NBD5 can produce lutein, and it is necessary to determine whether there is a new 52 pathway of lutein. In this study, the whole genome sequencing of Sphingopyxis USTB- 53 05 and Sphingomonas morindae NBD5 were performed for the first time. Lutein 54 synthesis metabolic pathways and synthetic genes were discovered in 55 Sphingomonadaceae. We predicted the existence of new lutein synthesis pathways and 56 revealed most of the genes of the new synthesis pathways. A comparative analysis of 57 the functional genes of the two strains revealed that Sphingopyxis USTB-05 contains a 58 large number of functional genes related to the biodegradation of hepatotoxins or 59 hexachlorocyclohexane. Among them, the functional genes related to the 60 biodegradation and metabolism of hexachlorocyclohexane had not been previously 61 reported. These findings lay the foundation for the biosynthesis of lutein using 62 Sphingomonas morindae NBD5 or Sphingopyxis USTB-05 and the application of 63 Sphingopyxis USTB-05 for the biodegradation of hepatotoxins microcystins and 64 nodularin or environmental pollutants. 65 66 INTRODUCTION 67 Lutein is a kind of carotenoid, which widely exits in vegetables, fruits and other plant. 68 It is also the main pigment in the macular area of human's eyes (1), and cannot be 69 synthesized by the body itself. Although it must be obtained from daily food, most 70 people's daily intake is seriously insufficient. The latest research showed that daily 71 intake of 10 mg lutein and 2 mg zeaxanthin could improve visual function and delay 72 the development of age-related macular degeneration (AMD) (2). Many researches 73 focused on the production of lutein by eukaryotes, and its synthesis pathway had been 74 clarified already. However, the production of lutein by prokaryotes was reported rarely. 75 The prokaryotic strains were only confined to some specific strains, for examples, 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 Erwinia, Agrobacterium and Rhodobacter capsulatus (2). Few research was reported 77 about Sphingomonas strains in lutein production. In our previous research, 78 Sphingomonas morindae NBD5 had the function of producing lutein (3). Phylogenetic 79 analysis showed that they belonged to two closely related genera of 80 Sphingomonadaceae (4) (5). 81 82 Sphingomonadaceae has a large number of strains that can biodegrade hepatotoxins or 83 environmental pollutants. In the 1990s, Sphingomonas wittichii RW1 was reported to 84 biodegrade dibenzo-p-dioxin (DD) polychlorinated derivatives under aerobic condition 85 in contaminated soil and water (6). Other types of Sphingomonas could also biodegrade 86 a series of intractable compounds (biphenyl, herbicide dichlorohaloperidin, γ- 87 hexachlorocyclohexane, aromatic hydrocarbons, chlorophenol, pentachlorophenol, 88 naphthalenesulfonic acid, N,N-dimethylaniline, diphenyl ether, dibenzofuran) that were 89 harmful to the environment (7). Hepatotoxins microcystins (MCs) and nodularin (NOD) 90 are derived from algae and have high toxicity and potential harm to humans and aquatic 91 animals. The World Health Organization (WHO) stipulated that the concentration of 92 MCs in drinking water should not be higher than 1.0 μg/L (8). Biodegradation is a very 93 promising method to remove hepatotoxins. At present, many strains of 94 Sphingomonadaceae family have the function of biodegrading hepatotoxins. However, 95 in order to fully clarify the metabolic process of biodegradation, new hepatotoxins 96 biodegradation genes need to be discovered. 97 98 Sphingomonas morindae NBD5 was a new species that was identified as this genus 99 only a few years ago (4). It could produce high yield of lutein, and the metabolic genes 100 needed further study. Sphingopyxis USTB-05 was isolated from Dianchi Lake in China 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 101 and could biodegrade MCs and NOD (5) (9) (10). These functional genes USTB-05-A, 102 USTB-05-B, and USTB-05-C of Sphingopyxis sp. USTB-05 had been verified by 103 heterologous expression in Escherichia coli to biodegrade MCs (11)(12). The purified 104 first recombinant enzyme was found to have a strong ability to catalyze hepatotoxins in 105 Sphingopyxis sp. USTB-05 (13). Because of the characteristics of lutein production and 106 hepatotoxin biodegradation of these two strains, the relationship between gene and 107 function was found through searching for functional genes. Here, the method of whole 108 genome combined with biometric analysis was used to compare the similar and unique 109 characteristics of Sphingomonas morindae NBD5 and Sphingopyxis USTB-05, and 110 analyze their functional genes, especially those associated with lutein synthesis and 111 hepatotoxin biodegradation. 112 113 RESULTS 114 General features of the nuclear genome 115 The Sphingomonas morindae NBD5 genome contained two circular chromosomes and 116 two circular plasmids (Figure 1). Polychromosomes were common in some genera, but 117 rare in Sphingomonas. Two circular chromosome of 4,239,716 bases was finally 118 obtained with a G + C content of 70%, and 3882 protein coding sequences (CDSs) were 119 predicted, accounting for 62.39% of the total coding sequence. The 16S rRNA of strain 120 NBD5 had 3 complete copies (Table 1). The Sphingopyxis USTB-05 genome contained 121 one chromosome (Figure 2). Its circular chromosome of 4,679,489 bases was finally 122 obtained with a G + C content of 64%, and 4312 CDSs were predicted, accounting for 123 62.39% of the total coding sequence. The 16S rRNA of strain USTB-05 was a single 124 copy (Table 1) without CRISPR site. Compared with strain USTB-05, the genome of 125 strain NBD5 was much richer in GC and contained plasmids, which indicated that some 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 126 genetic transfer events happened in strain NBD5 (Table 1). The number of functional 127 genes annotated in strain NBD5 was much more than that in strain USTB-05, but the 128 chromosome length of strain USTB-05 was longer than that of strain NBD5. 129 130 131 Figure 1 Genome circle of Sphingomonas morindae NBD5 6 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.29.437629; this version posted March 31, 2021.
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