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Plasmids Encode Niche-Specific Traits in Lactobacillaceae Dimple Davray, Dipti Deo and Ram Kulkarni* Symbiosis School of Biolog

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Plasmids Encode Niche-Specific Traits in Lactobacillaceae Dimple Davray, Dipti Deo and Ram Kulkarni* Symbiosis School of Biolog bioRxiv preprint doi: https://doi.org/10.1101/2020.08.20.258673; this version posted October 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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 Plasmids encode niche-specific traits in Lactobacillaceae 2 3 Dimple Davray, Dipti Deo and Ram Kulkarni* 4 5 Symbiosis School of Biological Sciences, Symbiosis International (Deemed University), Lavale, 6 Pune 412115, India 7 8 *Corresponding Author 9 Dr. Ram Kulkarni 10 [email protected] or [email protected]; 11 Tel.: +91 2028116477 12 13 Keywords: Lactobacillaceae, plasmid-encoded trait, ecological niche, comparative genomics, 14 stress resistance genes, Clusters of Orthologous Groups 15 16 bioRxiv preprint doi: https://doi.org/10.1101/2020.08.20.258673; this version posted October 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder.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. 17 Abstract 18 The species of family Lactobacillaceae are found in highly diverse environments and play an 19 important role in fermented foods and probiotic products. Many of these species have been 20 individually reported to harbor plasmids that encode important genes. In this study, we 21 performed comparative genomic analysis of the publically available data of 512 plasmids from 22 282 strains represented by 51 species of this family and correlated the genomic features of 23 plasmids with the ecological niches in which these species are found. Two-third of the species 24 had at least one plasmid-harboring strain. Plasmid abundance and GC content were significantly 25 lower in the vertebrate-adapted species as compared to the nomadic and free-living species. 26 Hierarchical clustering (HCL) highlighted the distinct nature of plasmids from the nomadic and 27 free-living species than those from the vertebrate-adapted species. EggNOG assisted functional 28 annotation revealed that genes associated with transposition, conjugation, DNA repair and 29 recombination, exopolysaccharide production, metal ion transport, toxin-antitoxin system, and 30 stress tolerance were significantly enriched on the plasmids of the nomadic and in some cases 31 nomadic and free-living species. On the other hand, genes related to anaerobic metabolism, ABC 32 transporters, and major facilitator superfamily were found to be overrepresented on the plasmids 33 of the vertebrate-adapted species. These genomic signatures are correlated to the comparatively 34 nutrient-depleted, stressful and dynamic environments of nomadic and free-living species and 35 nutrient-rich and anaerobic environments of the vertebrate-adapted species. Thus, these results 36 indicate the contribution of the plasmids in the adaptation of lactobacilli to the respective 37 habitats. This study also underlines the potential application of these plasmids in improving the 38 technological and probiotic properties of lactic acid bacteria. bioRxiv preprint doi: https://doi.org/10.1101/2020.08.20.258673; this version posted October 30, 2020. 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. 39 Impact statement 40 The bacteria of the family Lactobacillaceae are present in the wide range of habitats and play an 41 important role in human health, fermented foods and chemical industries. A few studies have 42 demonstrated the presence of plasmids in the individual strains of Lactobacillaceae species 43 encoding various traits. Extensive data of genome sequences of the lactobacilli are becoming 44 available; however, no comprehensive analysis of the plasmid-encoded genes and determining 45 their biological relevance across lactobacilli has been undertaken at a larger scale. In this study, 46 we explored the genomic content of 512 plasmids of Lactobacillaceae species and correlated it 47 to the three types of these species according to their ecological niches – vertebrate-adapted, free- 48 living and nomadic. Comparatively lower plasmid abundance and GC content in the vertebrate- 49 adapted species could be correlated to the presence of these species in the nutrient-rich 50 environment. The genomic content of the plasmids was consistent with the respective lifestyle 51 adopted by lactobacilli suggesting that the plasmids might enhance the niche-specific fitness of 52 the strains. The plethora of important genes present on the plasmids can also make them a highly 53 useful tool in improving the probiotic, technological and food-related properties of lactobacilli. 54 Data summary 55 Nucleotide sequences of plasmids of Lactobacillus strains for which complete genome sequences 56 were available were retrieved from the NCBI genome [https://www.ncbi.nlm.nih.gov/genome] 57 and PATRIC 3.5.41 databases on 31st March 2019. The dataset includes 512 nucleotide 58 sequences of plasmids of 282 strains belonging to genus Lactobacillus before its reclassification 59 into several genera (1). Details of the plasmids have been given in Table S1. bioRxiv preprint doi: https://doi.org/10.1101/2020.08.20.258673; this version posted October 30, 2020. 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. 60 1. Introduction 61 Lactobacilli are gram-positive, aerotolerant, and non-sporulating bacteria which belong to the 62 lactic acid bacteria (LAB) group wherein lactic acid is the major metabolic end product during 63 glucose fermentation (2). Lactobacillus is a major genus of the Lactobacillaceae family and the 64 highly diverse nature of its species has recently resulted in reclassification of this genus into 23 65 genera (1). Many lactobacilli have been associated with humans in a variety of ways. Their 66 presence in the gastrointestinal tract has earned extraordinary attention due to the health- 67 promoting properties of few of the genera. These bacteria are also important in the food industry 68 for the production of fermented dairy products wherein these bacteria provide the taste, texture, 69 and antibacterial activity (3). Furthermore, lactobacilli have applications in the production of 70 industrially important chemicals such as lactic acid (4). 71 Lactobacilli have been isolated from a wide range of habitats and have been found to 72 have highly diverse traits. Based on the properties such as phylogenetic analysis, source of 73 isolation, the prevalence of detection, optimal growth temperature, substrate utilization, and 74 environmental stress tolerance, the species of the earlier Lactobacillus genus have been classified 75 as host-adapted, nomadic and free-living (5). Some of the genomic features of these species are 76 correlated with these habitats. For example, the vertebrate-adapted lactobacilli (VAL) have 77 undergone genome reduction by losing a substantial number of genes involved in carbohydrate 78 metabolism and amino acid and cofactor biosynthesis because they thrive in a nutrient-rich 79 environment (5), (6), (7). On the other hand, free-living lactobacilli (FLL) and nomadic 80 lactobacilli (NL) have larger genome sizes because they encode various enzymes which utilize a 81 broad spectrum of carbohydrates (8). Furthermore, Lactobacillus helvticus DPC4571 and 82 Lactobacillus acidophilus NCFM were found to have genes important for the adaptation to their bioRxiv preprint doi: https://doi.org/10.1101/2020.08.20.258673; this version posted October 30, 2020. 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. 83 habitats, viz., dairy and gut, respectively (9). Lastly, Lactiplantibacillus plantarum, a hallmark 84 NL species found in most diverse habitats was also observed to have a highly diverse genome 85 with no unique environmental signature (10). Another classification of lactobacilli is based on 86 the carbohydrate fermentation pathways, as homofermentative and heterofermentative. In the 87 homofermentative species, the phosphotransferase system (PTS) is preferred to transport the 88 sugars which are fermented via the Emden-Meyerhoff pathway. On the other hand, in the 89 heterofermentative species, PTS are not functional and the phosphoketolase pathway is the 90 preferred catabolic pathway (11), (12). 91 Plasmids have been extensively found in lactobacilli and reported to carry the genes that 92 give them favorable traits and permit them to survive in competitive surroundings (13). Many 93 plasmids have been sequenced from the individual strains and found to encode important 94 functions such as oxidative stress response, antibiotic resistance, bacteriophage resistance, 95 chloride and potassium transport, and bacteriocin production (14), (15). Only a handful of reports 96 are available on the importance of plasmids in the niche adaptation of lactobacilli. In L. 97 plantarum P-8 isolated from fermented dairy products, loss of the plasmids important for dairy- 98 adaptation was found when the strain was administered in rats and humans (16). A plasmid from 99 Lacticaseibacillus paracasei NFBC338 isolated from the human gut encoded a gene involved in 100 adherence to the human intestinal epithelial cells (17). In Levilactobacillus brevis, the brewery 101 isolates were found to have the unique genes on the plasmids supporting the growth under the 102 harsh
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