Unexpected diversity in populations of the many‐celled magnetotactic prokaryote

Abstract

The many-celled magnetotactic prokaryote (MMP) is an uncultivated, highly motile aggregate of 10-30 cells containing numerous chains of greigite (Fe(3)S(4)) magnetosomes. It is unique to marine environments and is abundant in slightly sulfidic sediments of the Little Sippewissett salt marsh (Falmouth, MA). We sequenced 16s rDNA genes from a natural population of MMP and found five lineages separated by at least 5% sequence divergence. Fluorescent in situ hybridization probes for three of these lineages showed significant variation in their relative abundances across a seasonal cycle in marsh productivity. The MMP should therefore be considered a separate genus in the delta-proteobacteria rather than a single species as previously thought. All cells in each aggregate express identical SSU rRNAs, suggesting that the aggregates are composed of a single MMP phylotype. This observation supports a model of the MMP as comprised of clonal cells which reproduce by binary fission of the aggregate.

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

“…There is one group of prokaryotes that are considered to spend their entire life cycle as multicellular organisms: the magnetotactic multicellular prokaryotes (MMPs) Simmons and Edwards, 2007;Wenter et al, 2009;Shapiro et al, 2011;. One MMP, known as Candidatus Magnetoglobus multicellularis, consists of an organized assemblage of genetically identical Gram-negative cells that contain greigite (Fe 3 S 4 ) magnetosomes , which are membrane-bound nano-sized magnetic particles used for orientation and navigation along magnetic field lines (Bazylinski and Frankel, 2004).…”

Common ancestry of iron oxide- and iron-sulfide-based biomineralization in magnetotactic bacteria

“…Greigite-producing MTB have not been cultured and include a group of morphologically similar multicellular magnetotactic prokaryotes affiliated with Deltaproteobacteria (Abreu et al, 2007;Simmons and Edwards, 2007) and large rod-shaped bacteria (Pó sfai et al, 1998a), whose phylogeny has not been studied in detail. One report suggests that at least one type of greigite-producing MTB is affiliated with the Gammaproteobacteria (Simmons et al, 2004).…”

“…However, some doubt has been raised regarding the true phylogenetic relationship of this organism (Amann et al, 2006) and the recent isolation of two new gammaproteobacterial rod-shaped MTB (Lefèvre et al, 2010b) suggests that the organism described by Simmons et al (2004) biomineralizes magnetite. Confirmed greigite-producing MTB whose 16S rRNA gene has been sequenced include only the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis and bacteria morphologically similar to it (Abreu et al, 2007;Simmons and Edwards, 2007). This microorganism consists of an assemblage of genetically identical, Gram-negative bacteria that are capable of collectively migrating along magnetic field lines because of the coordinated rotation of flagella that cover each cell on one side.…”

Occurrence and microscopic analyses of multicellular magnetotactic prokaryotes from coastal sediments in the Yellow Sea

“…These microbes, named magnetotactic bacteria (MTB) are widespread in freshwater and marine environments and diverse in morphology, such as rods, vibrios, spirilla, cocci, giant rods and multicellular MTB (Faivre et al, 2008). Multicellular MTB were first found in 1983 in the Rodrigo de Freitas lagoon in Brazil (Farina et al, 1983), then in other coastal lagoons in Brazil, in stratified water column and coastal salt marshes in New England, in Mediterranean coastal sediments and in tidal sand flats of the North Sea Mann et al, 1990b;Rodgers et al, 1990;Delong et al, 1993;Keim et al, 2004a;Lefe Ávre et al, 2007;Simmons et al, 2007;Wenter et al, 2009). These organisms have been denominated differently in history, e.g., magnetotactic multicellular aggregate , many-celled magnetotactic prokaryote (Rodgers et al, 1990;Simmons et al, 2007) or multicellular magnetotactic prokaryote (Keim et al, 2004a;Lins et al, 2007;Winklhofer et al, 2007).…”

“…Rosette-like MMPs are spherical aggregates consisting of 7±45 gramnegative cells arranged in a helical way and flagellated on the outer surface (Keim et al, 2004a;Silva et al, 2007). Phylogenetic analysis reveals that all MMPs belong to d-Proteobacteria and cells within a MMP are of the same phylotype (Simmons et al, 2007;Wenter et al, 2009). MMPs synthesize mainly iron sulfide crystals Mann et al, 1990b;Delong et al, 1993;Po  sfai et al, 1998a;Po  sfai et al, 1998b) or/and magnetite .…”