Three Novel Species with Peptidoglycan Cell Walls Form the New Genus Gen. Nov. in the Family Opitutaceae of the Verrucomicrobial Subdivision 4

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2017 Mar 1

PMID 28243229

Citations 32

Authors

Patrick Rast

Ines Glockner

Christian Boedeker

Olga Jeske

Sandra Wiegand

Richard Reinhardt

Peter Schumann

Manfred Rohde

Stefan Spring

Frank O Glockner

Christian Jogler

Mareike Jogler

Affiliations

Soon will be listed here.

Abstract

The cell wall of free-living bacteria consists of peptidoglycan (PG) and is critical for maintenance of shape as dissolved solutes cause osmotic pressure and challenge cell integrity. Surprisingly, the subdivision 4 of the phylum Verrucomicrobia appears to be exceptional in this respect. Organisms of this subdivision are described to be devoid of muramic or diaminopimelic acid (DAP), usually found as components of PG in bacterial cell walls. Here we describe three novel bacterial strains from a freshwater lake, IG15, IG16b, and IG31, belonging to a new genus in the subdivision 4 of Verrucomicrobia which we found to possess PG as part of their cell walls. Biochemical analysis revealed the presence of DAP not only in these novel strains, but also in PB90-1, the closest described relative of strains IG15, IG16b, and IG31. Furthermore, we found that nearly all genes necessary for peptidoglycan synthesis are present in genomes of subdivision 4 members, as well as in the complete genome sequence of strain IG16b. In addition, we isolated and visualized PG-sacculi for strain IG16b. Thus, our results challenge the concept of peptidoglycan-less free-living bacteria. Our polyphasic taxonomy approach places the novel strains in a new genus within the family , for which the name gen. nov. is proposed. Strain designations for IG15, IG16b and IG31 are sp. nov. (=DSM 26814 = LMG 29468), sp. nov. (=DSM 26815 = LMG 29469) and sp. nov. (=DSM 103142 = LMG 29578) respectively, with IG16b being the type species of the genus.

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References

Pruesse E, Peplies J, Glockner F . SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012; 28(14):1823-9. PMC: 3389763. DOI: 10.1093/bioinformatics/bts252. View

Spring S, Bunk B, Sproer C, Schumann P, Rohde M, Tindall B . Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum. ISME J. 2016; 10(12):2801-2816. PMC: 5148204. DOI: 10.1038/ismej.2016.84. View

Chin K, Liesack W, Janssen P . Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division 'Verrucomicrobia' isolated from rice paddy soil. Int J Syst Evol Microbiol. 2002; 51(Pt 6):1965-1968. DOI: 10.1099/00207713-51-6-1965. View

van Passel M, Kant R, Palva A, Copeland A, Lucas S, Lapidus A . Genome sequence of the verrucomicrobium Opitutus terrae PB90-1, an abundant inhabitant of rice paddy soil ecosystems. J Bacteriol. 2011; 193(9):2367-8. PMC: 3133072. DOI: 10.1128/JB.00228-11. View

Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar . ARB: a software environment for sequence data. Nucleic Acids Res. 2004; 32(4):1363-71. PMC: 390282. DOI: 10.1093/nar/gkh293. View

Wang G, Huang X, Ng T, Lin J, Ye X . High phylogenetic diversity of glycosyl hydrolase family 10 and 11 xylanases in the sediment of Lake Dabusu in China. PLoS One. 2014; 9(11):e112798. PMC: 4231106. DOI: 10.1371/journal.pone.0112798. View

Zhou Y, Liang Y, Lynch K, Dennis J, Wishart D . PHAST: a fast phage search tool. Nucleic Acids Res. 2011; 39(Web Server issue):W347-52. PMC: 3125810. DOI: 10.1093/nar/gkr485. View

Packiam M, Weinrick B, Jacobs Jr W, Maurelli A . Structural characterization of muropeptides from Chlamydia trachomatis peptidoglycan by mass spectrometry resolves "chlamydial anomaly". Proc Natl Acad Sci U S A. 2015; 112(37):11660-5. PMC: 4577195. DOI: 10.1073/pnas.1514026112. View

Seemann T . Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014; 30(14):2068-9. DOI: 10.1093/bioinformatics/btu153. View

10.

van Teeseling M, Pol A, Harhangi H, van der Zwart S, Jetten M, Op den Camp H . Expanding the verrucomicrobial methanotrophic world: description of three novel species of Methylacidimicrobium gen. nov. Appl Environ Microbiol. 2014; 80(21):6782-91. PMC: 4249049. DOI: 10.1128/AEM.01838-14. View

11.

Jacquier N, Viollier P, Greub G . The role of peptidoglycan in chlamydial cell division: towards resolving the chlamydial anomaly. FEMS Microbiol Rev. 2015; 39(2):262-75. DOI: 10.1093/femsre/fuv001. View

12.

Schleifer K, Joseph R . A directly cross-linked L-ornithine-containing peptidoglycan in cell walls of Spirochaeta stenostrepta. FEBS Lett. 1973; 36(1):83-6. DOI: 10.1016/0014-5793(73)80342-4. View

13.

Valentine R, SHAPIRO B, Stadtman E . Regulation of glutamine synthetase. XII. Electron microscopy of the enzyme from Escherichia coli. Biochemistry. 1968; 7(6):2143-52. DOI: 10.1021/bi00846a017. View

14.

Pilhofer M, Rappl K, Eckl C, Bauer A, Ludwig W, Schleifer K . Characterization and evolution of cell division and cell wall synthesis genes in the bacterial phyla Verrucomicrobia, Lentisphaerae, Chlamydiae, and Planctomycetes and phylogenetic comparison with rRNA genes. J Bacteriol. 2008; 190(9):3192-202. PMC: 2347405. DOI: 10.1128/JB.01797-07. View

15.

Dhillon B, Laird M, Shay J, Winsor G, Lo R, Nizam F . IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res. 2015; 43(W1):W104-8. PMC: 4489224. DOI: 10.1093/nar/gkv401. View

16.

Rivas-Marin E, Canosa I, Devos D . Evolutionary Cell Biology of Division Mode in the Bacterial -- Superphylum. Front Microbiol. 2016; 7:1964. PMC: 5147048. DOI: 10.3389/fmicb.2016.01964. View

17.

Poole K . Resistance to beta-lactam antibiotics. Cell Mol Life Sci. 2004; 61(17):2200-23. PMC: 11138534. DOI: 10.1007/s00018-004-4060-9. View

18.

Miles R . Catabolism in mollicutes. J Gen Microbiol. 1992; 138(9):1773-83. DOI: 10.1099/00221287-138-9-1773. View

19.

Kim M, Pak S, Rim S, Ren L, Jiang F, Chang X . Luteolibacter arcticus sp. nov., isolated from high Arctic tundra soil, and emended description of the genus Luteolibacter. Int J Syst Evol Microbiol. 2015; 65(Pt 6):1922-1928. DOI: 10.1099/ijs.0.000202. View

20.

Lechner M, Findeiss S, Steiner L, Marz M, Stadler P, Prohaska S . Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics. 2011; 12:124. PMC: 3114741. DOI: 10.1186/1471-2105-12-124. View