Abstract
A Gram-negative strain, anaerobic, non-motile, non-spore-forming, rod-shaped bacterial strain named as NGMCC 1.200684 T was isolated from the fresh feces of rhinoceros in Beijing Zoo. Based on 16S rRNA gene sequences, phylogenetic analysis indicated that strain NGMCC 1.200684 T belonged to the genus Bacteroides and was most strongly related to the type strain of Bacteroides uniformis ATCC 8492 T (96.88%). The G + C content of the genomic DNA was determined to be 46.62%. Between strains NGMCC 1.200684 T and B. uniformis ATCC 8492 T, the average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) were 93.89 and 67.60%, respectively. Strain NGMCC 1.200684 T can produce acid from fermentation of several substrates, including glucose, mannitol, lactose, saccharose, maltose, salicin, xylose, cellobiose, mannose, raffinose, sorbitol, trehalose, D˗galactose, and maltotriose. The major cellular fatty acids (> 10%) were identified as anteiso˗C15:0, iso˗C15:0, iso˗C14:0, and iso˗C17:0 3˗OH. The polar lipid profiles of strain NGMCC 1.200684 T were determined to contain diphosphatidyl glycerol, phosphatidylglycerol, phosphatidylethanolamine, three unknown phospholipids, and two unknown amino-phospholipids. Based on phenotypic, phylogenetic, and chemotaxonomic characteristics, a novel species of the genus Bacteroides, Bacteroides rhinocerotis sp. nov. is proposed. The type strain is NGMCC 1.200684 T (= CGMCC 1.18013 T = JCM 35702 T).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The GenBank accession number for 16S rRNA gene sequences of strains NGMCC 1.200684 T is OP931997. The draft genome sequences of strains NGMCC 1.200684 T have been deposited at NCBI under the accession no. JAPDHT000000000.
References
Auch AF, von Jan M, Klenk H-P, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand in Genomic Sci 2:117–134. https://doi.org/10.4056/sigs.531120
Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH (2020) GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36:1925–1927. https://doi.org/10.1093/bioinformatics/btz848
Chen X, Li Q-Y, Li G-D, Lei H, Jiang Y, Han L, Huang X-S, Jiang C-L (2017) Enterovirga rhinocerotis gen. nov., sp. nov., isolated from Rhinoceros unicornis faeces. Antonie Van Leeuwenhoek 110:553–562. https://doi.org/10.1007/s10482-016-0823-1
Clavel T, Saalfrank A, Charrier C, Haller D (2010) Isolation of bacteria from mouse caecal samples and description of Bacteroides sartorii sp. nov. Arch Microbiol 192:427–435. https://doi.org/10.1007/s00203-010-0568-6
Endo A, Futagawa-Endo Y, Dicks LMT (2010) Diversity of Lactobacillus and Bifidobacterium in feces of herbivores, omnivores and carnivores. Anaerobe 16:590–596. https://doi.org/10.1016/j.anaerobe.2010.10.005
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Fokt H, Unni R, Repnik U, Schmitz RA, Bramkamp M, Baines JF, Unterweger D (2022) Bacteroides muris sp. nov. isolated from the cecum of wild-derived house mice. Arch Microbiol 204:1–10. https://doi.org/10.1007/s00203-022-03148-6
Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307. https://doi.org/10.1146/annurev.nutr.22.011602.092259
Irisawa T, Saputra S, Kitahara M, Sakamoto M, Sulistiani YT, Dinoto A, Ohkuma M (2016) Bacteroides caecicola sp. nov. and Bacteroides gallinaceum sp. nov., isolated from the caecum of an Indonesian chicken. Int J Syst Evol Microbiol 66:1431–1437. https://doi.org/10.1099/ijsem.0.000899
Kim HS, Kim JS, Suh MK, Eom MK, Lee JH, Park SH, Kang SW, Lee DH, Yoon H (2022) Bacteroides humanifaecis sp. nov., isolated from faeces of healthy Korean. Arch Microbiol 204:1–8. https://doi.org/10.1007/s00203-022-02967-x
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kitahara M, Tsuchida S, Kawasumi K, Amao H, Sakamoto M, Benno Y, Ohkuma M (2011) Bacteroides chinchillae sp. nov. and Bacteroides rodentium sp. nov., isolated from chinchilla (Chinchilla lanigera) faeces. Int J Syst Evol Microbiol 61:877–881. https://doi.org/10.1099/ijs.0.024026-0
Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Biol 18:1–32. https://doi.org/10.1093/sysbio/18.1.1
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651. https://doi.org/10.1126/science.1155725
Li GD, Chen X, Li QY, Xu FJ, Qiu SM, Jiang Y, Jiang CL (2015) Sphingobacterium rhinocerotis sp. nov., isolated from the faeces of Rhinoceros unicornis. Antonie Van Leeuwenhoek 108:1099–1105. https://doi.org/10.1007/s10482-015-0563-7
Li GD, Chen X, Li QY, Xu FJ, Qiu SM, Jiang Y, Jiang CL (2016) Tessaracoccus rhinocerotis sp. nov., isolated from the faeces of Rhinoceros unicornis. Int J Syst Evol Microbiol 66:922–927. https://doi.org/10.1099/ijsem.0.000812
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:1–14. https://doi.org/10.1186/1471-2105-14-60
Minnikin DE, Abdolrahimzadeh H (1974) Effect of pH on the proportions of polar lipids, in chemostat cultures of Bacillus subtilis. J Bacteriol 120:999–1003. https://doi.org/10.1128/jb.120.3.999-1003.1974
Nishiyama T, Ueki A, Kaku N, Watanabe K, Ueki K (2009) Bacteroides graminisolvens sp. nov., a xylanolytic anaerobe isolated from a methanogenic reactor treating cattle waste. Int J Syst Evol Microbiol 59:1901–1907. https://doi.org/10.1099/ijs.0.008268-0
Parks DH, Chuvochina M, Waite DW et al (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. https://doi.org/10.1038/nbt.4229
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sakamoto M, Ohkuma M (2013) Bacteroides reticulotermitis sp. nov., isolated from the gut of a subterranean termite (Reticulitermes speratus). Int J Syst Evol Microbiol 63:691–695. https://doi.org/10.1099/ijs.0.040931-0
Sakamoto M, Suzuki M, Umeda M, Ishikawa I, Benno Y (2002) Reclassification of Bacteroides forsythus as Tannerella forsythensis corrig., gen. nov., comb. nov. Int J Syst Evol Microbiol 52:841–849
Saputra S, Irisawa T, Sakamoto M, Kitahara M, Sulistiani YT, Ohkuma M, Dinoto A (2015) Bacteroides caecigallinarum sp. nov., isolated from caecum of an Indonesian chicken. Int J Syst Evol Microbiol 65:4341–4346. https://doi.org/10.1099/ijsem.0.000573
Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC News 20:1–6
Shah HN (1992) The genus Bacteroides and related taxa. In: Albert B, Hans GT, Martin D, Wim H, Karl-Heinz S (eds) The Prokaryotes. Springer, New York
Shah HN, Collins MD (1980) Fatty acid and isoprenoid quinone composition in the classification of Bacteroides melaninogenicus and related taxa. J Appl Bacteriol 48:75–87. https://doi.org/10.1111/j.1365-2672.1980.tb05209.x
Shah HN, Collins MD (1983) Genus Bacteroides a chemotaxonomical perspective. J Appl Bacteriol 55:403–416. https://doi.org/10.1111/j.1365-2672.1983.tb01680.x
Shah HN, Collins MDY (1989) Proposal to restrict the genus Bacteroides (Castellani and Chalmers) to Bacteroides fragilis and closely related species. Int J Syst Evol Microbiol 39:85–877. https://doi.org/10.1099/00207713-39-1-85
Smith CJ, Rocha ER, Paster BJ (2006) The medically important Bacteroides spp. in health and disease. In: Dworkin M, Falkow S, Rosenberg E et al (eds) The Prokaryotes: Volume 7: Proteobacteria: Delta, Epsilon Subclass. Springer, New York, pp 381–427
Sonnenburg JL, Angenent LT, Gordon JI (2004) Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 5:569–573. https://doi.org/10.1038/ni1079
Sun XW, Abdugheni R, Huang HJ, Wang YJ, Jiang MZ, Liu C, Zhou N, Jiang H (2022) Bacteroides propionicigenes sp nov, isolated from human faeces. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.005397
Tan H, Zhao J, Zhang H, Zhai Q, Chen W (2019) Novel strains of Bacteroides fragilis and Bacteroides ovatus alleviate the LPS-induced inflammation in mice. Appl Microbiol Biotechnol 103:2353–2365. https://doi.org/10.1007/s00253-019-09617-1
Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut Bacteroidetes: the food connection. Front Microbiol. https://doi.org/10.3389/fmicb.2011.00093
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Tittsler RP, Sandholzer LA (1936) The use of semi-solid agar for the getection of bacterial motility. J Bacteriol 31:575–580. https://doi.org/10.1128/jb.31.6.575-580.1936
Tsuchida S, Ushida K (2015) Characterization of intestinal bacterial communities of western lowland gorillas ( Gorilla gorilla gorilla ), central chimpanzees (Pan troglodytes troglodytes ), and a forest elephant (Loxodonta africana cyclotis ) living in Moukalaba-Doudou National Par. Tropics 23:175–183. https://doi.org/10.3759/tropics.23.175
Ueki A, Abe K, Kaku N, Watanabe K, Ueki K (2008) Bacteroides propionicifaciens sp. nov., isolated from rice-straw residue in a methanogenic reactor treating waste from cattle farms. Int J Syst Evol Microbiol 58:346–352. https://doi.org/10.1099/ijs.0.65486-0
Ueki A, Abe K, Ohtaki Y, Kaku N, Watanabe K (2011) Bacteroides paurosaccharolyticus sp. nov., isolated from a methanogenic reactor treating waste from cattle farms. Int J Syst Evol Microbiol 61:448–453. https://doi.org/10.1099/ijs.0.022566-0
Wang C, Zhao J, Zhang H, Lee Y-K, Zhai Q, Chen W (2021) Roles of intestinal bacteroides in human health and diseases. Crit Rev Food Sci Nutr 61:3518–3536. https://doi.org/10.1080/10408398.2020.1802695
Wayne LG (1988) International committee on systematic bacteriology: announcement of the report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Syst Appl Microbiol 10:99–100. https://doi.org/10.1016/S0723-2020(88)80020-1
Wexler HM (2007) Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev 20:593–621. https://doi.org/10.1128/CMR.00008-07
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yu SY, Kim JS, Oh BS, Park SH, Kang SW, Park JE, Choi SH, Han KI, Lee KC (2019) Bacteroides faecalis sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 69:3824–3829. https://doi.org/10.1099/ijsem.0.003690
Funding
This research was supported by the National Key Research and Development Program of China (2021YFF0702900), CAMS initiative for Innovative Medicine of China (2021-I2M-1-039, 2021-I2M-1-034), and the open fund of Key Laboratory of Microbial Resources Collection and Preservation, Ministry of Agriculture and Rural Affairs (KLMRCP2021-09).
Author information
Authors and Affiliations
Contributions
XL and LS carried out the data analysis, wrote, and revised the manuscript. XL, PLS, LG, and WXS performed the experiments. ZGX and ML participated in the data analysis. LS and CQ supervised the project. All authors reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Ethics approval and consent to participate
In this study, the collection and the analysis of animal feces did not involve animal ethics.
Additional information
Communicated by Wen-Jun Li.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
203_2023_3513_MOESM1_ESM.tif
Supplementary file 1 (TIF 3748 KB)—Fig. S1. Scanning electron micrographs of strain NGMCC 1.200684T. Cells were grown on mGAM medium at 37°C for 72 h. Bar, 2 μm and 5μm.
203_2023_3513_MOESM2_ESM.tif
Supplementary file 2 (TIF 4042 KB)—Fig. S2. Analysis of the COG function classification (A), and analysis of the KEGG function classification (B) based on the genomes of stain NGMCC 1.200684T.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, X., Sun, P., Gong, L. et al. Bacteroides rhinocerotis sp. nov., isolated from the fresh feces of rhinoceros in Beijing Zoo. Arch Microbiol 205, 169 (2023). https://doi.org/10.1007/s00203-023-03513-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-023-03513-z