Nonmagnetotactic Multicellular Prokaryotes from Low-Saline, Nonmarine Aquatic Environments and Their Unusual Negative Phototactic Behavior

Abstract

Magnetotactic multicellular prokaryotes (MMPs) are unique magnetotactic bacteria of the Deltaproteobacteria class and the first found to biomineralize the magnetic mineral greigite (Fe 3 S 4 ). Thus far they have been reported only from marine habitats. We questioned whether MMPs exist in low-saline, nonmarine environments. MMPs were observed in samples from shallow springs in the Great Boiling Springs geothermal field and Pyramid Lake, both located in northwestern Nevada. The temperature at all sites was ambient, and salinities ranged from 5 to 11 ppt. These MMPs were not magnetotactic and did not contain magnetosomes (called nMMPs here). nMMPs ranged from 7 to 11 m in diameter, were composed of about 40 to 60 Gram-negative cells, and were motile by numerous flagella that covered each cell on one side, characteristics similar to those of MMPs. 16S rRNA gene sequences of nMMPs show that they form a separate phylogenetic branch within the MMP group in the Deltaproteobacteria class, probably representing a single species. nMMPs exhibited a negative phototactic behavior to white light and to wavelengths of <480 nm (blue). We devised a "light racetrack" to exploit this behavior, which was used to photoconcentrate nMMPs for specific purposes (e.g., DNA extraction) even though their numbers were low in the sample. Our results show that the unique morphology of the MMP is not restricted to marine and magnetotactic prokaryotes. Discovery of nonmagnetotactic forms of the MMP might support the hypothesis that acquisition of the magnetosome genes involves horizontal gene transfer. To our knowledge, this is the first report of phototaxis in bacteria of the Deltaproteobacteria class.One of the most interesting and unusual examples of prokaryotic morphology is that of the organism known as the magnetotactic multicellular prokaryote (MMP; also known as the magnetotactic multicellular aggregate [MMA] [16,37] and the magnetotactic multicellular organism [MMO] [30]). The acronym MMP originally stood for many-celled magnetotactic prokaryote (45,46,53,54), but in more recent reports, because of a number of recent findings suggesting that individual cells interact and/or communicate with each other, many investigators use MMP for multicellular magnetotactic prokaryote (for an example, see reference 59).

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

“…In all cases, the salinity is due to the input of seawater, and many have considered these organisms indigenous to marine environments only (44). Recently, nonmagnetotactic forms of MMPs (referred to as nMMPs) were found in springs and lakes with relatively low salinities (ϳ5 to 11 ppt) and no marine input (80). Little is known regarding their physiology, but it seems very likely that MMPs and nMMPs are sulfate-reducing bacteria based on the facts that their closest phylogenetic relatives are sulfate reducers (43,44) (Fig.…”

“…7A). This clade is composed of several genera of multicellular organisms having variable sizes and morphologies, biomineralizing either magnetite, greigite, or both (43)(44)(45)121) or, in the case of the nMMPs, known not to biomineralize magnetosomes (80). The closest relatives of the MMPs are species of the genera Desulfosarcina, Desulfonema, and Desulfococcus.…”

“…MMPs are cosmopolitan in distribution, being found in numerous saline aquatic environments ranging from brackish to hypersaline (19,42,80,124,132). In all cases, the salinity is due to the input of seawater, and many have considered these organisms indigenous to marine environments only (44).…”

“…Some MMPs and nonmagnetotactic multicellular prokaryotes (nMMPs) show a strong negative phototactic response to white light and wavelengths of light of Յ480 nm (74,79,80). Because shorter wavelengths of light of Յ480 nm (blue to violet) are those that generally penetrate the water column the deepest (81), this negative phototactic response might function similarly to magnetotaxis, in that if light causes MMPs and nMMPs in nature to swim more or less vertically downward, then, like magnetotaxis (5), it would at least partially reduce a three-dimensional search problem to a one-dimensional search problem for an organism that must locate and maintain an optimal position in vertical chemical and redox gradients common in aquatic habitats.…”

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

“…Because of the presence of several light receptorrelated genes in the partial genome of Ca. M. multicellularis, microscopic observations of environmental samples and previous studies (Lefèvre et al, 2010;Shapiro et al, 2011), Ca. M. multicellularis appears to also use light for orientation in addition to magnetoaerotaxis and chemotaxis.…”