Gen. Nov., Sp. Nov., and Sp. Nov., Two Marine Anaerobes of the Fam. Nov. Producing Sulfated Glycosaminoglycan-like Exopolymers

Overview

Journal Microorganisms

Specialty Microbiology

Date 2020 Jun 24

PMID 32570748

Citations 7

Authors

Daan M van Vliet

Yuemei Lin

Nicole J Bale

Michel Koenen

Laura Villanueva

Alfons J M Stams

Irene Sanchez-Andrea

Affiliations

Soon will be listed here.

Abstract

Recently, we isolated two marine strains, F1 and F21, which together with L21-Fru-AB are the only pure cultures of the class within the phylum Here, we present an in-depth genome-guided characterization of both isolates with emphasis on their exopolysaccharide synthesis. The strains only grew fermentatively on simple carbohydrates and sulfated polysaccharides. Strains F1, F21 and reduced elemental sulfur, ferric citrate and anthraquinone-2,6-disulfonate during anaerobic growth on sugars. Both strains produced exopolysaccharides during stationary phase, probably with intracellularly stored glycogen as energy and carbon source. Exopolysaccharides included N-sulfated polysaccharides probably containing hexosamines and thus resembling glycosaminoglycans. This implies that the isolates can both degrade and produce sulfated polysaccharides. Both strains encoded an unprecedently high number of glycoside hydrolase genes (422 and 388, respectively), including prevalent alpha-L-fucosidase genes, which may be necessary for degrading complex sulfated polysaccharides such as fucoidan. Strain F21 encoded three putative glycosaminoglycan sulfotransferases and a putative sulfate glycosaminoglycan biosynthesis gene cluster. Based on phylogenetic and chemotaxonomic analyses, we propose the taxa F1 gen. nov., sp. nov. and F21 sp. nov. as representatives of the fam. nov. within the class .

Citing Articles

Discovering Hidden Archaeal and Bacterial Lipid Producers in a Euxinic Marine System.

Boukhchtaber D, von Meijenfeldt F, Sahonero Canavesi D, Dorhout D, Bale N, Hopmans E Environ Microbiol. 2025; 27(3):e70054.

PMID: 40016913 PMC: 11868695. DOI: 10.1111/1462-2920.70054.

A deep-sea isopod that consumes sinking from the ocean's surface.

Peoples L, Gerringer M, Weston J, Leon-Zayas R, Sekarore A, Sheehan G Proc Biol Sci. 2024; 291(2030):20240823.

PMID: 39255840 PMC: 11387067. DOI: 10.1098/rspb.2024.0823.

Organic matter degradation in the deep, sulfidic waters of the Black Sea: insights into the ecophysiology of novel anaerobic bacteria.

Yadav S, Koenen M, Bale N, Reitsma W, Engelmann J, Stefanova K Microbiome. 2024; 12(1):98.

PMID: 38797849 PMC: 11129491. DOI: 10.1186/s40168-024-01816-x.

sp. nov., a novel marine anaerobic bacterium capable of degrading macroalgal polysaccharides and fixing nitrogen.

Liu N, Kivenson V, Peng X, Cui Z, Lankiewicz T, Gosselin K Appl Environ Microbiol. 2024; 90(2):e0091423.

PMID: 38265213 PMC: 10880615. DOI: 10.1128/aem.00914-23.

Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in fish.

Oliver A, Podell S, Wegley Kelly L, Sparagon W, Plominsky A, Nelson R bioRxiv. 2023; .

PMID: 38076955 PMC: 10705383. DOI: 10.1101/2023.11.28.568905.

References

Ollivier B, Caumette P, Garcia J, Mah R . Anaerobic bacteria from hypersaline environments. Microbiol Rev. 1994; 58(1):27-38. PMC: 372951. DOI: 10.1128/mr.58.1.27-38.1994. View

Felz S, Neu T, van Loosdrecht M, Lin Y . Aerobic granular sludge contains Hyaluronic acid-like and sulfated glycosaminoglycans-like polymers. Water Res. 2019; 169:115291. DOI: 10.1016/j.watres.2019.115291. View

Duval S, Ducluzeau A, Nitschke W, Schoepp-Cothenet B . Enzyme phylogenies as markers for the oxidation state of the environment: the case of respiratory arsenate reductase and related enzymes. BMC Evol Biol. 2008; 8:206. PMC: 2500031. DOI: 10.1186/1471-2148-8-206. View

Bienkowski M, Conrad H . Structural characterization of the oligosaccharides formed by depolymerization of heparin with nitrous acid. J Biol Chem. 1985; 260(1):356-65. View

. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 2018; 47(D1):D506-D515. PMC: 6323992. DOI: 10.1093/nar/gky1049. View

Rodriguez-R L, Gunturu S, Harvey W, Rossello-Mora R, Tiedje J, Cole J . The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res. 2018; 46(W1):W282-W288. PMC: 6031002. DOI: 10.1093/nar/gky467. View

Thrash J, Cho J, Vergin K, Morris R, Giovannoni S . Genome sequence of Lentisphaera araneosa HTCC2155T, the type species of the order Lentisphaerales in the phylum Lentisphaerae. J Bacteriol. 2010; 192(11):2938-9. PMC: 2876483. DOI: 10.1128/JB.00208-10. View

Tanaka T, Kawasaki K, Daimon S, Kitagawa W, Yamamoto K, Tamaki H . A hidden pitfall in the preparation of agar media undermines microorganism cultivability. Appl Environ Microbiol. 2014; 80(24):7659-66. PMC: 4249246. DOI: 10.1128/AEM.02741-14. View

Bale N, Sorokin D, Hopmans E, Koenen M, Rijpstra W, Villanueva L . New Insights Into the Polar Lipid Composition of Extremely Halo(alkali)philic Euryarchaea From Hypersaline Lakes. Front Microbiol. 2019; 10:377. PMC: 6423904. DOI: 10.3389/fmicb.2019.00377. View

10.

Sanchez-Andrea I, Florentino A, Semerel J, Strepis N, Sousa D, Stams A . Co-culture of a Novel Fermentative Bacterium, gen. nov. sp. nov., With the Sulfur Reducer for Enhanced Sulfidogenesis. Front Microbiol. 2019; 9:3108. PMC: 6315149. DOI: 10.3389/fmicb.2018.03108. View

11.

Wegner C, Richter-Heitmann T, Klindworth A, Klockow C, Richter M, Achstetter T . Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics. 2013; 9:51-61. DOI: 10.1016/j.margen.2012.12.001. View

12.

Wittmann J, Dreiseikelmann B, Rohde M, Meier-Kolthoff J, Bunk B, Rohde C . First genome sequences of Achromobacter phages reveal new members of the N4 family. Virol J. 2014; 11:14. PMC: 3915230. DOI: 10.1186/1743-422X-11-14. View

13.

Wasmund K, Mussmann M, Loy A . The life sulfuric: microbial ecology of sulfur cycling in marine sediments. Environ Microbiol Rep. 2017; 9(4):323-344. PMC: 5573963. DOI: 10.1111/1758-2229.12538. View

14.

Giordano A, Vella F, Romano I, Gambacorta A . Structural elucidation of a novel phosphoglycolipid isolated from six species of Halomonas. J Lipid Res. 2007; 48(8):1825-31. DOI: 10.1194/jlr.M700152-JLR200. View

15.

Rubin-Blum M, Antony C, Sayavedra L, Martinez-Perez C, Birgel D, Peckmann J . Fueled by methane: deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts. ISME J. 2019; 13(5):1209-1225. PMC: 6474228. DOI: 10.1038/s41396-019-0346-7. View

16.

Khadem A, van Teeseling M, van Niftrik L, Jetten M, Op den Camp H, Pol A . Genomic and Physiological Analysis of Carbon Storage in the Verrucomicrobial Methanotroph "Ca. Methylacidiphilum Fumariolicum" SolV. Front Microbiol. 2012; 3:345. PMC: 3460235. DOI: 10.3389/fmicb.2012.00345. View

17.

Yu N, Wagner J, Laird M, Melli G, Rey S, Lo R . PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010; 26(13):1608-15. PMC: 2887053. DOI: 10.1093/bioinformatics/btq249. View

18.

Benz , Schink , BRUNE . Humic acid reduction by propionibacterium freudenreichii and other fermenting bacteria . Appl Environ Microbiol. 1998; 64(11):4507-12. PMC: 106677. DOI: 10.1128/AEM.64.11.4507-4512.1998. View

19.

Burdige D, Nealson K . Microbial manganese reduction by enrichment cultures from coastal marine sediments. Appl Environ Microbiol. 1985; 50(2):491-7. PMC: 238648. DOI: 10.1128/aem.50.2.491-497.1985. View

20.

Cardman Z, Arnosti C, Durbin A, Ziervogel K, Cox C, Steen A . Verrucomicrobia are candidates for polysaccharide-degrading bacterioplankton in an arctic fjord of Svalbard. Appl Environ Microbiol. 2014; 80(12):3749-56. PMC: 4054139. DOI: 10.1128/AEM.00899-14. View