Insight into the Evolution of Magnetotaxis in Magnetospirillum spp., Based on mam Gene Phylogeny

Abstract

c Vibrioid-to helical-shaped magnetotactic bacteria phylogenetically related to the genus Magnetospirillum were isolated in axenic cultures from a number of freshwater and brackish environments located in the southwestern United States. Based on 16S rRNA gene sequences, most of the new isolates represent new Magnetospirillum species or new strains of known Magnetospirillum species, while one isolate appears to represent a new genus basal to Magnetospirillum. Partial sequences of conserved mam genes, genes reported to be involved in the magnetosome and magnetosome chain formation, and form II of the ribulose-1,5-bisphosphate carboxylase/oxygenase gene (cbbM) were determined in the new isolates and compared. The cbbM gene was chosen for comparison because it is not involved in magnetosome synthesis; it is highly conserved and is present in all but possibly one of the genomes of the magnetospirilla and the new isolates. Phylogenies based on 16S rRNA, cbbM, and mam gene sequences were reasonably congruent, indicating that the genes involved in magnetotaxis were acquired by a common ancestor of the Magnetospirillum clade. However, in one case, magnetosome genes might have been acquired through horizontal gene transfer. Our results also extend the known diversity of the Magnetospirillum group and show that they are widespread in freshwater environments. Magnetotactic bacteria (MTB) are a metabolically, morphologically, and phylogenetically heterogeneous group of aquatic prokaryotes that passively align and actively swim along magnetic field lines (3). This behavior, termed magnetotaxis, is due to the presence of intracellular single-magnetic-domain crystals of magnetite (Fe 3 O 4 ) and/or greigite (Fe 3 S 4 ) surrounded by a lipid bilayer. These unique structures, called magnetosomes, are generally organized into a chain(s) within the cell and impart a permanent magnetic dipole to the cell, resulting in the cells' magnetotactic behavior (3). MTB are ubiquitous in aquatic habitats typified by the presence of oxygen concentrations and redox gradients in the water column or sediments (3).Among the MTB, members of the genus Magnetospirillum are the most studied and well understood in terms of the biomineralization of magnetite and the construction of the magnetosome chain. Most of this knowledge is based on the genetic analysis of two species: Magnetospirillum gryphiswaldense strain MSR-1 (35) and M. magneticum strain AMB-1 (31). Three Magnetospirillum species are well characterized. The genome of M. magneticum strain AMB-1 has been completed, and while most of the genomes of M. gryphiswaldense strain MSR-1 and M. magnetotacticum strain MS-1 have been sequenced, they have not yet been closed as a chromosome (8,29). Known magnetotactic Magnetospirillum species are facultatively anaerobic microaerophiles that biomineralize a chain of cuboctahedral crystals of magnetite, although some strains do not produce magnetosomes (e.g., M. bellicus [45]). Morphologically, all known Magnetospirillum species are helical and are bipolarl...

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

“…Ms. gryphiswaldense is also capable of autotrophic and mixotrophic growth using reduced sulfur compounds as a source of electrons (51). Although the pathway of autotrophy was not determined, it seems likely that carbon dioxide fixation occurs through the Calvin-Benson-Bassham (CBB) cycle, since a form II ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) gene was found in the genomes of Ms. magnetotacticum (87) and other Magnetospirillum-related strains (64). While most species are facultative anaerobes that utilize nitrate as an alternative terminal electron acceptor to oxygen, Ms. magnetotacticum appears to be an obligate microaerophile that requires oxygen even when growing with nitrate (98,99).…”

“…The first involves the formation of individual colonies. This has been achieved by using agar plates of appropriate media such as activated charcoal agar (ACA) (64,65). This technique has proven effective in growing Magnetospirillum and related freshwater MTB on solid medium.…”

“…Considering the very close phylogenetic relationship between Phaeospirillum, Dechlorospirillum, and Magnetospirillum, it would be necessary to modify the classification of the branch grouping those genera by including the Phaeospirillum and Dechlorospirillum species in the genus Magnetospirillum or by dividing members of the genus Magnetospirillum into several different genera (Fig. 4A) (60,64). Indeed, the genus Phaeospirillum contains spiral-shaped, phototrophic, purple nonsulfur bacterial species (105), a physiological trait that is not shared with species of the genus Magnetospirillum, although the presence of intracellular membranes is common to both Phaeospirillum (105) and magnetosome-forming Magnetospirillum species.…”

Diversity of <i>Magnetospirillum</i> Sp. from the Southern Coast of India

“…The distribution of mam genes in strains M.VITRJS2 and M.VITRJS5 was found to be similar to the two well-characterized strains M. gryphiswaldense (MSR1) and Magnetospirillum magneticum (AMB1) and previously isolated strain Magnetospirillum sp. VITRJS1, whereas the absence of two important mam genes (mamD and mamF) in strain M.VITRJS6 shows the divergence of the evolution of strain from the others 28 . The role of Mam proteins in magnetosome biomineralization is well studied and these putative functions include magnetosome vesicle formation (MamA and MamF), iron transportation (MamB, MamC and MamM), crystal structure formation (MamD), chain formation (MamJ and MamK) and protein sorting (MamQ) 33 .…”

“…Maximum number of MTB has been previously reported from the top sediment. Therefore, top ~5 cm of sediment that includes and surrounds the OAI was collected 5,28 . The limnological characteristics of the samples such as temperature and pH were analysed (Table 1).…”