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Paludisphaera soli sp. nov., a new member of the family Isosphaeraceae isolated from high altitude soil in the Western Himalaya

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Abstract

A novel strain of Planctomycetes, designated JC670T, was isolated from a high altitude (~ 2900 m above sea level) soil sample collected from Garhwal region in the Western Himalaya. Colonies of this strain were observed to be light pink coloured with spherical to oval shaped cells having crateriform structures distributed all over the cell surface. The cells divide by budding. Strain JC670T was found to grow well at pH 7.0 and pH 8.0 and to tolerate up to 2% NaCl (w/v). MK6 was the only respiratory quinone identified. The major fatty acids of strain JC670T were identified as C18:1ω9c, C18:0 and C16:0, and phosphatidylcholine, two unidentified phospholipids and six unidentified lipids are present as the polar lipids. The polyamines putrescine and sym-homospermidine were detected. Strain JC670T shows high 16S rRNA gene sequence identity (95.4%) with Paludisphaera borealis PX4T. The draft genome size of strain JC670T is 7.97 Mb, with G + C content of 70.4 mol%. Based on phylogenetic analyses with the sequences of ninety-two core genes, low dDDH value (20.6%), low gANI (76.8%) and low AAI (69.1%) results, differential chemotaxonomic and physiological properties, strain JC670T (= KCTC 72850T = NBRC 114339T) is recognised as the type strain of a new species of the genus Paludisphaera, for which we propose the name Paludisphaera soli sp. nov.

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Abbreviations

NCBI:

National Center for Biotechnology Information

ANI:

Average Nucleotide Index

AAI:

Average Nucleotide Index

dDDH:

Digital DNA-DNA Hybridization

HPLC:

High-Pressure Liquid Chromatography

KCTC:

Korean Collection for Type Cultures

References

  • Auch AF, Klenk HP, Göker M (2010) Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2:142–148

    PubMed  PubMed Central  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M et al (2008) The RAST server: rapid annotations using subsystems technology. BMC genomics 9:75

    PubMed  PubMed Central  Google Scholar 

  • Baghel VS, Tripathi RD, Ramteke PW, Gopal K, Dwivedi S, Jain RK, Rai UN, Singh SN (2005) Psychrotrophic proteolytic bacteria from cold environment of Gangotri glacier, Western Himalaya, India. Enzyme Microb Tech 36:654–659

    CAS  Google Scholar 

  • Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bondoso J, Albuquerque L, Nobre MF, Lobo-da-Cunha A, da Costa MS, Lage OM (2011) Aquisphaera giovannonii gen. nov., sp. nov., a planctomycete isolated from a freshwater aquarium. Int J Syst Evol Microbiol 61:2844–2850

    CAS  PubMed  Google Scholar 

  • Bondoso J, Albuquerque L, Nobre MF, Lobo-da-Cunha A, da Costa MS, Lage OM (2015) Roseimaritima ulvae gen. nov., sp. nov. and Rubripirellula obstinate gen. nov., sp. nov. two novel planctomycetes isolated from the epiphytic community of macroalgae. Syst Appl Microbiol 38:8–15

    PubMed  Google Scholar 

  • Borneman J, Skroch PW, O'Sullivan KM, Palus JA, Rumjanek NG, Jansen JL, Nienhuis J, Triplett EW (1996) Molecular microbial diversity of an agricultural soil in Wisconsin. Appl Environ Microbiol 62:1935–1943

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borneman J, Triplett EW (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63:2647–2653

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buckley DH, Huangyutitham V, Nelson TA, Rumberger A, Thies JE (2006) Diversity of planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl Environ Microbiol 72:4522–4531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, Meyer SD, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    CAS  PubMed  Google Scholar 

  • Darzi Y, Letunic I, Bork P, Yamada T (2018) iPath3. 0: interactive pathways explorer v3. Nucleic Acids Res 46:W510–W513

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dedysh SN, Ivanova AA (2019) Planctomycetes in boreal and subarctic wetlands: diversity patterns and potential ecological functions. FEMS Microbiol Eco 95:fiy227

    CAS  Google Scholar 

  • Dedysh SN, Kulichevskaya IS, Beletsky AV, Ivanova AA, Rijpstra WIC, Damsté JSS, Ravin NV (2020) Lacipirellula parvulagen. nov., sp. nov., representing a lineage of planctomycetes widespread in low-oxygen habitats, description of the family Lacipirellulaceae fam. nov. and proposal of the orders Pirellulalesord. nov., Gemmatalesord. nov. and Isosphaerales ord. nov. Syst Appl Microbiol 43:126050

    PubMed  PubMed Central  Google Scholar 

  • Eisenreich W, Bacher A, Arigoni D, Rohdich F (2004) Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61:1401–1426

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Imhoff JF (1984) Quinones of phototrophic purple bacteria. FEMS Microbiol Lett 25:85–89

    CAS  Google Scholar 

  • Ivanova AO, Dedysh SN (2012) Abundance, diversity, and depth distribution of planctomycetes in acidic northern wetlands. Front Microbiol 3:5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanova AA, Naumoff DG, Miroshnikov KK, Liesack W, Dedysh SN (2017) Comparative genomics of four Isosphaeraceae planctomycetes: a common pool of plasmids and glycoside hydrolase genes shared by Paludisphaera borealis PX4T, Isosphaera pallida IS1BT, Singulisphaera acidiphila DSM 18658T, and strain SH-PL62. Front Microbiol 8:412

    PubMed  PubMed Central  Google Scholar 

  • Jogler C, Wiegand S, Boedeker C, Heuer A, Peeters SH, Jogler M, Jetten MSM, Rohde M, Kallscheuer N (2020) Tautonia plasticadhaerens sp. nov., a novel species in the family Isosphaeraceae isolated from an alga in a hydrothermal area of the Eolian Archipelago. Antonie van Leeuwenhoek. https://doi.org/10.1007/s10482-020-01424-3

  • Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kates M (1972) Isolation, analysis and identification of lipids. Tech Lipidol 3:268–618

    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

    CAS  PubMed  Google Scholar 

  • Köhler T, Stingl U, Meuser K, Brune A (2008) Novel lineages of Planctomycetes densely colonize the alkaline gut of soil-feeding termites (Cubitermes spp.). Environ Microbiol 10:1260–1270

    PubMed  Google Scholar 

  • Kulichevskaya IS, Ivanova AA, Suzina NE, Rijpstra WIC, Damste JSS, Dedysh SN (2016) Paludisphaera borealis gen. nov., sp. nov., a hydrolytic planctomycete from northern wetlands, and proposal of Isosphaeraceae fam. nov. Int J Syst Evol Microbiol 66:837–844

    CAS  PubMed  Google Scholar 

  • Kumar D, Gaurav K, Uppada J, Deepshikha G, Ch S, Ch VR (2020a) Roseimaritima sediminicola sp. nov., a new member of Planctomycetaceae isolated from Chilika lagoon. Int J Syst Evol Microbiol 70:2616–2623

    CAS  PubMed  Google Scholar 

  • Kumar D, Gaurav K, Sreya PK, Shabbir A, Uppada J, Sasikala Ch, Ramana CV (2020b) Gimesia chilikensis sp. nov., a haloalkali-tolerant planctomycete isolated from Chilika lagoon and emended description of the genus Gimesia. Int J Syst Evol Microbiol 70:3647–3655

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  • Kumar S, Suyal DC, Yadav A, Shouche Y, Goel R (2019) Microbial diversity and soil physiochemical characteristic of higher altitude. PLoS ONE 14:e0213844

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mac Faddin JF (1985) Media for isolation-cultivation-identification-maintenance of medical bacteria. Williams & Wilkins, Philadelphia

    Google Scholar 

  • Mc Inerney JO, Martin WF, Koonin EV, Allen JF, Galperin MY, Lane N, Embley AJM, TM, (2011) Planctomycetes and eukaryotes: a case of analogy not homology. BioEssays 33:810–817

    CAS  Google Scholar 

  • Meier-Kolthoff JP, Klenk HP, Göker M (2014) Taxonomic use of DNA G+ C content and DNA–DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352–356

    CAS  PubMed  Google Scholar 

  • Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J (2018) UBCG: Up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285

    CAS  PubMed  Google Scholar 

  • Neef A, Amann R, Schlesner H, Schleifer KH (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144:3257–3266

    CAS  PubMed  Google Scholar 

  • Oren A, Duker S, Ritter S (1996) The polar lipid composition of Walsby's square bacterium. FEMS Microbiol Lett 138:135–140

    CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rodriguez-R LM, Konstantinidis KT (2016) The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes (No. e1900v1). Peer J Preprints

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids.

  • Stackebrandt E, Liesack W, Goebel BM (1993) Bacterial diversity in a soil sample from a subtropical Australian environment as determined by 16S rDNA analysis. FASEB J 7:232–236

    CAS  PubMed  Google Scholar 

  • Wagner M, Horn M (2006) The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol 17:241–249

    CAS  PubMed  Google Scholar 

  • Wang J, Jenkins C, Webb RI, Fuerst JA (2002) Isolation of Gemmata-like and Isosphaera-like planctomycete bacteria from soil and freshwater. Appl Environ Microbiol 68:417–422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T, Bun C, Conrad N, Dietrich EM, Disz T, Gabbard JL, Gerdes S, Henry CS, Kenyon RW et al (2017) Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45:D535–D542

    CAS  PubMed  Google Scholar 

  • Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PloS Comput Biol 13:e1005595

    PubMed  PubMed Central  Google Scholar 

  • Wiegand S, Jogler M, Jogler C (2018) On the maverick Planctomycetes. FEMS Microbiol Rev 42:739–760

    CAS  PubMed  Google Scholar 

  • Wiegand S, Jogler M, Boedeker C, Pinto D, Vollmers J, Rivas-Marín E, Oberbeckmann S et al (2020) Cultivation and functional characterization of 79 Planctomycetes uncovers their unique biology. Nat Microbiol 5:126–140

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Chang WC, Xiao Y, Liu HW, Liu P (2013) Methylerythritol phosphate pathway of isoprenoid biosynthesis. Annu Rev Biochem 82:497–530

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

MS thanks CSIR, RK and KG thank the DBT, New Delhi and JU thanks TEQIP III for the award for research fellowships. Ramana thanks the Department of Biotechnology, Government of India for the award of Tata Innovation fellowship. Sasikala thanks UGC for Mid-Career Award. We thank the staff and the laboratory facilities provided by Centre for Interdisciplinary Studies of Mountain & Hill Environment, University of Delhi.

Funding

This work received grant specifically from Department of Biotechnology, Government of India. Financial support received from Council for Scientific and Industrial Research (CSIR), and AICTE, New Delhi is acknowledged. Infrastructure facilities funded by DST-FIST, UGC-SAP (DRS) and TEQIP, AICTE-RPS and MODROBS are acknowledged. The financial assistance of DST-PURSE Grant to MKP is gratefully acknowledged.

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Author notes

  1. Rishabh Kaushik and Meesha Sharma having equal authorship and consider as first authors.

Authors and Affiliations

  1. Department of Environmental Studies, University of Delhi, Delhi, 110007, India

    Rishabh Kaushik, Meesha Sharma & Maharaj K. Pandit

  2. Department of Plant Sciences, School of Life Sciences, University of Hyderabad, P.O. Central University, Hyderabad, 500046, India

    Kumar Gaurav, A. Shabbir & Ch. V. Ramana

  3. Bacterial Discovery Laboratory, Centre for Environment, Institute of Science and Technology, J. N. T. University Hyderabad, Kukatpally, Hyderabad, 500085, India

    U. Jagadeeshwari & Ch. Sasikala

Authors
  1. Rishabh Kaushik
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Contributions

RK and MS performed sample collection. RK, MS and KG isolated the strain and performed the initial cultivation, strain deposition and strain characterisation, KG performed the electron microscopic analysis and media optimisation, JU performed the genomic and phylogenetic analysis, SA performed and analysed the data for polyamines, RK, MS and KG wrote the manuscript, Ramana, Sasikala and MKP supervised the study and contributed to text preparation and revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Ch. V. Ramana or Maharaj K. Pandit.

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Kaushik, R., Sharma, M., Gaurav, K. et al. Paludisphaera soli sp. nov., a new member of the family Isosphaeraceae isolated from high altitude soil in the Western Himalaya. Antonie van Leeuwenhoek 113, 1663–1674 (2020). https://doi.org/10.1007/s10482-020-01471-w

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