Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

Abstract

Candidatus Magnetoglobus multicellularis (Ca. M. multicellularis) is a member of a group of uncultured magnetotactic prokaryotes that possesses a unique multicellular morphology. To better understand this organism's physiology, we used a genomic approach through pyrosequencing. Genomic data analysis corroborates previous structural studies and reveals the proteins that are likely involved in multicellular morphogenesis of this microorganism. Interestingly, some detected protein sequences that might be involved in cell adhesion are homologues to phylogenetically unrelated filamentous multicellular bacteria proteins, suggesting their contribution in the early development of multicellular organization in Bacteria. Genes related to the behavior of Ca. M. multicellularis (chemo-, photo-and magnetotaxis) and its metabolic capabilities were analyzed. On the basis of the genomic-physiologic information, enrichment media were tested. One medium supported chemoorganoheterotrophic growth of Ca. M. multicellularis and allowed the microorganisms to maintain their multicellular morphology and cell cycle, confirming for the first time that the entire life cycle of the MMP occurs in a multicellular form. Because Ca. M. multicellularis has a unique multicellular life style, its cultivation is an important achievement for further studies regarding the multicellular evolution in prokaryotes.

Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment

“…For the Deltaproteobacteria , complete genome sequences are available for Desulfovibrio magneticus strain RS-1 [12]. Partial genomic information is also available for other cultured MTB affiliated with the Alphaproteobacteria [13, 14] and cultured and uncultured MTB belonging to the Deltaproteobacteria [15–18], Nitrospirae [19, 20], Candidatus Omnitrophica (part of the Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) bacterial superphylum) [19] and possibly to the Latescibacteria [21, 22]. These partial genomic sequences include descriptions of mam genes for characterization of biomineralization processes in MTB except for the Latescibacterial SCGC AAA252-B13 genome which was used for the identification of an uncultured environmental microorganism [21] and for the detection of mam gene homology without characterization of morphological features of this putative MTB [22].…”

A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China

“…M. multicelluaris (Abreu et al ., ). It has been proposed that MMPs use phototaxis in combination with chemotaxis and aerotaxis to follow daily changes in the vertical distribution of nutrients (Lefèvre et al ., ; Shapiro et al ., ; Abreu et al ., ). Based on the similar swimming behaviour observed for the novel ellipsoidal MMPs, we infer that their genome should possess these hallmark genes.…”

On the evolution of bacterial multicellularity

“…The tetrahedral-shaped cells are arranged in a single layer with their flagellated base facing the environment and their narrower ends facing inward [30,31], creating an apparently hollow cavity reminiscent of the Volvocaceae algae [32]. By electron microscopy the cells of an MMP appear to be connected by tight intercellular junctions similar to animal epithelia [33], and dislodgement of any individual cells leads to loss of motility, suggesting these organisms can only function as a multicellular unit [30]. MMPs have been observed to reproduce by fission of the whole organism without going through a unicellular state [23,24,28], making it the only known example of a bacterium without a unicellular phase in its lifecycle.…”

“…These include extracellular matrixes composed of polysaccharides, nucleic acids, and proteins [19]; quorum sensing-mediated triggering of multicellular states [15]; control by regulatory molecules such as cyclic di-GMP, signaling kinases, and phosphate-binding domains [52–54]; transmembrane adhesion proteins [33]; and the presence of spores or spore-like cells [50]. Complicating the matter of conservation is widespread horizontal gene transfer throughout the microbial world, which some have suggested may play a bigger role in bacterial evolution than classic mechanisms like gene duplication [55].…”