Magnetospirillum caucaseum sp. nov., Magnetospirillum marisnigri sp. nov. and Magnetospirillum moscoviense sp. nov., freshwater magnetotactic bacteria isolated from three distinct geographical locations in European Russia
Three strains of helical, magnetotactic bacteria, SO-1T, SP-1T and BB-1T, were isolated from freshwater sediments collected from three distinct locations in European Russia. Phylogenetic analysis showed that the strains belong to the genus Magnetospirillum. Strains SO-1T and SP-1T showed the highest 16S rRNA gene sequence similarity to Magnetospirillum magnetotacticum MS-1T (99.3 and 98.1 %, respectively), and strain BB-1T with Magnetospirillum gryphiswaldense MSR-1T (97.3 %). The tree based on concatenated deduced amino acid sequences of the MamA, B, K, M, O, P, Q and T proteins, which are involved in magnetosome formation, was congruent with the tree based on 16S rRNA gene sequences. The genomic DNA G+C contents of strains SO-1T, SP-1T and BB-1T were 65.9, 63.0 and 65.2 mol%, respectively. As major fatty acids, C18 : 1ω9, C16 : 1ω7c, C16 : 0 and C18 : 0 were detected. DNA–DNA hybridization values between the novel strains and their closest relatives in the genus Magnetospirillum were less than 51.7 ± 2.3 %. In contrast to M. magnetotacticum MS-1T, the strains could utilize butyrate and propionate; strains SO-1T and BB-1T could also utilize glycerol. Strain SP-1T showed strictly microaerophilic growth, whereas strains SO-1T and BB-1T were more tolerant of oxygen. The results of DNA–DNA hybridization and physiological tests allowed genotypic and phenotypic differentiation of the strains from each other as well as from the two species of Magnetospirillum with validly published names. Therefore, the strains represent novel species, for which we propose the names Magnetospirillum caucaseum sp. nov. (type strain SO-1T = DSM 28995T = VKM B-2936T), Magnetospirillum marisnigri sp. nov. (type strain SP-1T = DSM 29006T = VKM B-2938T) and Magnetospirillum moscoviense sp. nov. (type strain BB-1T = DSM 29455T = VKM B-2939T).
AraujoA.C.V.,
AbreuF.,
SilvaK. T.,
BazylinskiD. A.,
LinsU.2015; Magnetotactic bacteria as potential sources of bioproducts. Mar Drugs 13:389–430 [View Article][PubMed]
BazylinskiD. A.,
DeanA. J.,
SchülerD.,
PhillipsE.J.P.,
LovleyD. R.2000; N2-dependent growth and nitrogenase activity in the metal-metabolizing bacteria, Geobacter and Magnetospirillum species. Environ Microbiol 2:266–273 [View Article][PubMed]
BlakemoreR. P.,
MarateaD.,
WolfeR. S.1979; Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol 140:720–729[PubMed]
BryantsevaI.,
GorlenkoV. M.,
KompantsevaE. I.,
ImhoffJ. F.,
SülingJ.,
MityushinaL.1999; Thiorhodospira sibirica gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium from a Siberian soda lake. Int J Syst Bacteriol 49:697–703 [View Article][PubMed]
BulyginaE. S.,
KuznetsovB. B.,
MarusinaA. I.,
TurovaT. P.,
KravchenkoI. K.,
BykovaS. A.,
KolganovaT. V.,
Gal'chenkoV. F.2002; [Study of nucleotide sequences of nifH genes in methanotrophic bacteria]. Mikrobiologiia 71:500–508 (in Russian)[PubMed]
De LeyJ.,
CattoirH.,
ReynaertsA.1970; The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142 [View Article][PubMed]
DziubaM. V.,
KolganovaT. V.,
GorlenkoV. M.,
KuznetsovB. B.2013; Species diversity of magnetotactic bacteria from the Ol'khovka River, Russia. Microbiology [English translation of Mikrobiologiia] 82:335–340 [View Article]
GorlenkoV. M.,
DziubaM. V.,
MaleevaA. N.,
PanteleevaA. N.,
KolganovaT. V.,
KuznetsovB. B.2011; [Magnetospirillum aberrantis sp. nov., a new freshwater bacterium with magnetic inclusions]. Mikrobiologiia 80:679–690 (in Russian)[PubMed]
HeyenU.,
SchülerD.2003; Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Appl Microbiol Biotechnol 61:536–544 [View Article][PubMed]
KonstantinidisK. T.,
RametteA.,
TiedjeJ. M.2006; Toward a more robust assessment of intraspecies diversity, using fewer genetic markers. Appl Environ Microbiol 72:7286–7293 [View Article][PubMed]
LefèvreC. T.,
SchmidtM. L.,
ViloriaN.,
TrubitsynD.,
SchülerD.,
BazylinskiD. A.2012; Insight into the evolution of magnetotaxis in Magnetospirillum spp., based on mam gene phylogeny. Appl Environ Microbiol 78:7238–7248 [View Article][PubMed]
LohßeA.,
UllrichS.,
KatzmannE.,
BorgS.,
WannerG.,
RichterM.,
VoigtB.,
SchwederT.,
SchülerD.2011; Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense: the mamAB operon is sufficient for magnetite biomineralization. PLoS One 6:e25561 [View Article][PubMed]
MarusinaA. I.,
BoulyginaE. S.,
KuznetsovB. B.,
TourovaT. P.,
KravchenkoI. K.,
Gal'chenkoV. F.2001; A system of oligonucleotide primers for the amplification of nifH genes of different taxonomic groups of prokaryotes. Microbiology [English translation of Mikrobiologiia] 70:73–78 [View Article]
MatsunagaT.,
SakaguchiT.,
TadokoroF.1991; Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol 35:651–655[CrossRef]
MuratD.,
QuinlanA.,
ValiH.,
KomeiliA.2010; Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc Natl Acad Sci U S A 107:5593–5598 [View Article][PubMed]
OwenR. J.,
HillL. R.,
LapageS. P.1969; Determination of DNA base compositions from melting profiles in dilute buffers. Biopolymers 7:503–516 [View Article][PubMed]
SchleiferK.-H.,
SchulerD.,
SpringS.,
WeizeneggerM.,
AmannR.,
LudwigW.,
KohlerM.1991; The genus Magnetospirillum gen. nov. Description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. Syst Appl Microbiol 14:379–385 [View Article]
SmalleyM. D.,
MarinovG. K.,
BertaniL. E.,
DeSalvoG.2015; Genome sequence of Magnetospirillum magnetotacticum strain MS-1. Genome Announc 3:e00233–e00215 [View Article][PubMed]
SpiridonovaE. M.,
BergI. A.,
KolganovaT. V.,
Ivanovskii˘R. N.,
KuznetsovB. B.,
TurovaT. P.2004; [An oligonucleotide primer system for amplification of the ribulose-1, 5-bisphosphate carboxylase/oxygenase genes of bacteria of various taxonomic groups]. Mikrobiologiia 73:377–387 (in Russian)[PubMed]
ThompsonJ. D.,
HigginsD. G.,
GibsonT. J.1994; clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [View Article][PubMed]
TindallB. J.,
Rosselló-MóraR.,
BusseH.-J.,
LudwigW.,
KämpferP.2010; Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266 [View Article][PubMed]
Magnetospirillum caucaseum sp. nov., Magnetospirillum marisnigri sp. nov. and Magnetospirillum moscoviense sp. nov., freshwater magnetotactic bacteria isolated from three distinct geographical locations in European Russia