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Description of Aureibaculum luteum sp. nov. and Aureibaculum flavum sp. nov. isolated from Antarctic intertidal sediments

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Abstract

Two Gram-stain-negative, aerobic, non-motile, and rod-shaped bacterial strains, designated SM1352T and A20T, were isolated from intertidal sediments collected from King George Island, Antarctic. They shared 99.8% 16S rRNA gene sequence similarity with each other and had the highest sequence similarity of 98.1% to type strain of Aureibaculum marinum but < 93.4% sequence similarity to those of other known bacterial species. The genomes of strains SM1352T and A20T consisted of 5,108,092 bp and 4,772,071 bp, respectively, with the G + C contents both being 32.0%. They respectively encoded 4360 (including 37 tRNAs and 6 rRNAs) and 4032 (including 36 tRNAs and 5 rRNAs) genes. In the phylogenetic trees based on 16S rRNA gene and single-copy orthologous clusters (OCs), both strains clustered with Aureibaculum marinum and together formed a separate branch within the family Flavobacteriaceae. The ANI and DDH values between the two strains and Aureibaculum marinum BH-SD17T were all below the thresholds for species delineation. The major cellular fatty acids (> 10%) of the two strains included iso-C15:0, iso-C15:1 G, iso-C17:0 3-OH. Their polar lipids predominantly included phosphatidylethanolamine, one unidentified aminophospholipid, one unidentified aminolipid, and two unidentified lipids. Genomic comparison revealed that both strains possessed much more glycoside hydrolases and sulfatase-rich polysaccharide utilization loci (PULs) than Aureibaculum marinum BH-SD17T. Based on the above polyphasic evidences, strains SM1352T and A20T represent two novel species within the genus Aureibaculum, for which the names Aureibaculum luteum sp. nov. and Aureibaculum flavum sp. nov. are proposed. The type strains are SM1352T (= CCTCC AB 2014243 T = JCM 30335 T) and A20T (= CCTCC AB 2020370 T = KCTC 82503 T), respectively.

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References

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbeyron T, Brillet-Guéguen L, Carré W, Carrière C, Caron C, Czjzek M, Hoebeke M, Michel G (2016) Matching the diversity of sulfated biomolecules: creation of a classification database for sulfatases reflecting their substrate specificity. PLoS One. 11:e0164846

    Article  PubMed  PubMed Central  Google Scholar 

  • Barbeyron T, Thomas F, Barbe V, Teeling H, Schenowitz C, Dossat C, Goesmann A, Leblanc C, Glöckner FO, Czjzek M (2016b) Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacte- ria: example of the model algae-associated bacterium Zobellia galactanivorans DsijT. Environ Microbiol 18:4610–4627

    Article  CAS  PubMed  Google Scholar 

  • Bennke CM, Krüger K, Kappelmann L, Huang S, Gobet A, Schüler M, BarbeV FBM, Michel G, Teeling H (2016) Polysaccharide utilisation loci of Bacteroidetes from two contrasting open ocean sites in the North Atlantic. Environ Microbiol 18:4456–4470

    Article  CAS  PubMed  Google Scholar 

  • Bowman JP (2006) The marine clade of the family Flavobacteriaceae: the genera Aequorivita, Arenibacter, Cellulophaga, Croceibacter, Formosa, Gelidibacter, Gillisia, Maribacter, Mesonia, Muricauda, Polaribacter, Psychroexus, Psychroserpens, Robiginitalea, Salegentibacter, Tenacibaculum, Ulvibacter, Vitellibacter and Zobellia. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The Prokaryotes: a Handbook on the Biology of Bacteria, vol 7, 3rd edn. Springer, New York, pp 677–694

    Chapter  Google Scholar 

  • Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    Article  CAS  PubMed  Google Scholar 

  • Collins MD, Jones D (1980) Lipids in the classification and identification of coryneform bacteria containing peptidoglycans based on 2,4-diaminobutyric acid. J Appl Bacteriol 48:459–470

    Article  CAS  Google Scholar 

  • Du ZZ, Zhou LY, Wang TJ, Li HR, Du ZJ (2020) Lutibacter citreus sp. nov., isolated from Arctic surface sediment. Int J Syst Evolution Microbiol 70:3154–3161

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Re 32:1792–1797

    Article  CAS  Google Scholar 

  • Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238

    Article  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Gomez B, Richter M, Schüler M, Pinhassi J, Acinas SG, González JM, Pedrós-Alió C (2013) Ecology of marine Bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037

    Article  PubMed  PubMed Central  Google Scholar 

  • Ficko-Blean E, Préchoux A, Thomas F, Rochat T, Larocque R, Zhu Y, Stam M, Génicot S, Jam M, Calteau A, Viart B, Ropartz D, Pérez-Pascual D, Correc G, Matard-Mann M, Stubbs KA, Rogniaux H, Jeudy A, Barbeyron T, Médigue C, Czjzek M, Vallenet D, McBride MJ, Duchaud E, Michel G (2017) Carrageenan catabolism is encoded by a complex regulon in marine heterotrophic bacteria. Nat Commun 8:1685

    Article  PubMed  PubMed Central  Google Scholar 

  • Hettle AG, Hobbs JK, Pluvinage B, Vickers C, Abe KT, Salama-Alber O, McGuire BE, Hehemann JH, Hui JPM, Berrue F, Banskota A, Zhang J, Bottos EM, Van Hamme J, Boraston AB (2019) Insights into the κ/ι-carrageenan metabolism pathway of some marine Pseudoalteromonas species. Commun Biol 2:474

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobbs JK, Lee SM, Robb M, Hof F, Barr C, Abe KT, Hehemann JH, McLean R, Abbott DW, Boraston AB (2016) KdgF, the missing link in the microbial metabolism of uronate sugars from pectin and alginate. Proc Natl Acad Sci USA 113:6188–6193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2019) EggNOG 05.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47(D1):D309–D314

    Article  CAS  PubMed  Google Scholar 

  • Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, Jahesh G, Khan H, Coombe L, Warren RL, Birol I (2017) ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res 27:768–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Komagata K, Suzuki K (1987) Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161–207

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lagesen K, Hallin P, Rødland EA, Stærfeldt HH, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lechner M, Findeiß S, Steiner L, Marz M, Stadler PF, Prohaska SJ (2011) Proteinortho: detection of (co-) orthologs in large-scale analysis. BMC Bioinf 12:124

    Article  Google Scholar 

  • Liu C, Zhang XY, Wen XR, Shi M, Chen XL, Su HN (2016) Arcticiflavibacter luteus gen. nov. sp. nov. a member of the family flavobacteriaceae isolated from intertidal sand. Int J Syst Evolut. Microbiol. 66:144–149

    Article  CAS  Google Scholar 

  • Liu J, Xue C, Sun H, Zheng Y, Meng Z, Zhang X (2019) Carbohydrate catabolic capability of a Flavobacteriia bacterium isolated from hadal water. Syst Appl Microbiol 42:263–274

    Article  CAS  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McBride MJ (2014) The family Flavobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes-Other Major Lineages of Bacteria and the Archaea, vol 11, 4th edn. Springer, Berlin, pp 643–676

    Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 14:60

    Article  Google Scholar 

  • Murray RGE, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 21–41

    Google Scholar 

  • Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin QL, **e BB, Zhang XY, Chen XL, Zhou BC, Zhou JZ, Oren A, Zhang YZ (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196:2210–2215

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118

    Google Scholar 

  • Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sasser M (2001) Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids, 101, MIDI Technical Note. Newark, DE: MIDI

  • Shieh WY, Lin YT, Jean WD (2004) Pseudovibrio denitrificans gen. nov., sp. nov., a marine, facultatively anaerobic, fermentative bacterium capable of denitrification. Int J Syst Evol Microbiol 54:2307–2312

    Article  CAS  PubMed  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  • Sun C, Fu G, Zhang C, Hu J, Xu L, Wang R, Su Y, Han S, Yu X, Cheng H (2016) Isolation and complete genome sequence of Algibacter alginolytica sp. nov., a novel seaweed-degrading Bacteroidetes bacterium with diverse putative polysaccharide utilization loci. Appl Environ Microb 82:2975–2987

    Article  CAS  Google Scholar 

  • Wang N, Xu F, Zhang XY, Chen XL, Qin QL, Zhou BC (2017) Changchengzhania lutea gen. nov., sp. nov., a new member of the family Flavobacteriaceae isolated from Antarctic intertidal sediment. Int J Syst Evol Microbiol 67:5187–5192

    Article  PubMed  Google Scholar 

  • **ng P, Hahnke RL, Unfried F, Markert S, Huang S, Barbeyron T, Harder J, Becher D, Schweder T, Glöckner FO, Amann RI, Teeling H (2015) Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom. ISME J 9:1410–1422

    Article  CAS  PubMed  Google Scholar 

  • Yoon SH, Ha SM, Kwon S, Lim J, KimY SH, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Li HR, Zeng YX, Sun K, Chen B (2012) Pricia antarctica gen. nov., sp. nov., a member of the family Flavobacteriaceae, isolated from Antarctic intertidal sediment. Int J Syst Evol Microbiol 62:2218–2223

    Article  PubMed  Google Scholar 

  • Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, Busk PK, Xu Y, Yin Y (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:95–101

    Article  CAS  Google Scholar 

  • Zhao HL, Wu YL, Zhang C, Feng JR, Xu Z, Ding YF, Gao YX, Geng Y, Song J, Li BQ, Ji XF (2019) Aureibaculum marinum gen. nov., sp. nov., a novel bacterium of the family Flavobacteriaceae isolated from the Bohai Gulf. Curr Microbiol 76:975–981

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We sincerely thank **g-yao Qu, **g Zhu and Zhi-feng Li from State Key Laboratory of Microbial Technology of Shandong University for help and guidance in LC-MS.

Funding

This work was supported by the National Key Research and Development Program of China (grants 2018YFC1406700, 2018YFC1406704, and 2018YFC0310704), the National Science Foundation of China (grants 91851205, 31630012, and 42076151), Major Scientific and Technological Innovation Project (MSTIP) of Shandong Province (2019JZZY010817), the Program of Shandong for Taishan Scholars (tspd20181203). Persons employed by the funders had no role in the study or in the preparation of the article or decision to publish.

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  1. State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, 266237, China

    **ao-yan He, Ning-hua Liu, Chao-yi Lin, **u-lan Chen, Yu-zhong Zhang, Yu-qiang Zhang & **-ying Zhang

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    **u-lan Chen, Yu-zhong Zhang & **-ying Zhang

  3. College of Marine Life Sciences, and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, 266003, China

    Mei-ling Sun & Yu-zhong Zhang

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**-ying Zhang designed the work. **ao-yan He, Chao-yi Lin, Ning-hua Liu and **-ying Zhang performed experiments, collected and analysed data. **ao-yan He, Yu-qiang Zhang and **-ying Zhang drafted the manuscript. **-ying Zhang, Mei-ling Sun, **u-lan Chen and Yu-zhong Zhang interpreted some data and revised the manuscript. All authors read and approved the final manuscript.

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He, Xy., Liu, Nh., Lin, Cy. et al. Description of Aureibaculum luteum sp. nov. and Aureibaculum flavum sp. nov. isolated from Antarctic intertidal sediments. Antonie van Leeuwenhoek 115, 391–405 (2022). https://doi.org/10.1007/s10482-021-01702-8

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