Genomic evidence of the illumination response mechanism and evolutionary history of magnetotactic bacteria within the Rhodospirillaceae family

Abstract

Background Magnetotactic bacteria (MTB) are ubiquitous in natural aquatic environments. MTB can produce intracellular magnetic particles, navigate along geomagnetic field, and respond to light. However, the potential mechanism by which MTB respond to illumination and their evolutionary relationship with photosynthetic bacteria remain elusive. Results We utilized genomes of the well-sequenced genus Magnetospirillum , including the newly sequenced MTB strain Magnetospirillum sp. XM-1 to perform a comprehensive genomic comparison with phototrophic bacteria within the family Rhodospirillaceae regarding the illumination response mechanism. First, photoreceptor genes were identified in the genomes of both MTB and phototrophic bacteria in the Rhodospirillaceae family, but no photosynthesis genes were found in the MTB genomes. Most of the photoreceptor genes in the MTB genomes from this family encode phytochrome-domain photoreceptors that likely induce red/far-red light phototaxis. Second, illumination also causes damage within the cell, and in Rhodospirillaceae, both MTB and phototrophic bacteria possess complex but similar sets of response and repair genes, such as oxidative stress response, iron homeostasis and DNA repair system genes. Lastly, phylogenomic analysis showed that MTB cluster closely with phototrophic bacteria in this family. One photoheterotrophic genus, Phaeospirillum , clustered within and displays high genomic similarity with Magnetospirillum . Moreover, the phylogenetic tree topologies of magnetosome synthesis genes in MTB and photosynthesis genes in phototrophic bacteria from the Rhodospirillaceae family were reasonably congruent with the phylogenomic tree, suggesting that these two traits were most likely vertically transferred during the evolution of their lineages. Conclusion Our new genomic data indicate that MTB and phototrophic bacteria within the family Rhodospirillaceae possess diversified photoreceptors that may be responsible for phototaxis. Their genomes also contain comprehensive stress response genes to mediate the negative effects caused by illumination. Based on phylogenetic studies, most of MTB and phototrophic bacteria in the Rhodospirillaceae family evolved vertically with magnetosome synthesis and photosynthesis genes. The ancestor of Rhodospirillaceae was likely a magnetotactic phototrophic bacteria, however, gain or loss of magnetotaxis and phototrophic abilities might have occurred during the evolution of ancestral Rhodospirillaceae lineages. Electronic supplementary material The online version of this article (10.1186/s12864-019-5751-9) contains supplementary material, which is available to authorized users.

Iron‐biomineralizing organelle in magnetotactic bacteria: function, synthesis and preservation in ancient rock samples

“…Genomic, environmental and ultrastructural evidences seem to indicate that the deep‐branched MTB including the Nitrospirae candidate genera Magnetobacterium (Jogler et al ., 2011; Lin et al ., 2014b; Kolinko et al ., 2016) and Magnetoovum (Lefèvre et al ., 2011a,b,c,d; Kolinko et al ., 2016) as well as some magnetotactic cocci of the Magnetococcaceae family isolated from the water column of the Black Sea (Schulz‐Vogt et al ., 2019) are growing anaerobically using nitrate as respiratory electron acceptor and oxidizing reduced sulfur compounds. Although some MTB have been shown to be sensitive to light (Frankel et al ., 1997; Chen et al ., 2011; Shapiro et al ., 2011) with genomic evidences supporting the presence of phototrophic genes in some Magnetospirillum strains (Wang et al ., 2019), no photosynthetic MTB have been found. So far, no MTB were shown to be able to use reduced or oxidized forms of iron for their energetic metabolism.…”

Repeated horizontal gene transfers triggered parallel evolution of magnetotaxis in two evolutionary divergent lineages of magnetotactic bacteria

“…Since their first observation, numerous other spirilla were isolated and affiliated to the same group based on phenotypic, physiological and morphological features, among which the ability to form magnetosomes [7][8][9][10][11]. As for many prokaryotes, the increasing biodiversity assessment and the development of molecular typing revealed the polyphyletism of magnetotaxis in freshwater Rhodospirillaceae (Alphaproteobacteria) [8,12]. Members of two genera with different lifestyles: Phaeospirillum and Dechlorospirillum are actually more closely related to some…”

“…Magnetospirillum lineages than what some Magnetospirillum lineages are to each other [7,8,12,13]. The genus Phaeospirillum contains spiral-shaped, phototrophic, purple nonsulphur bacterial species [14], while Dechlorospirillum, now affiliated to the Magnetospirillum genus based on phylogenetic analyses, is represented by non-MTB only [15,16].…”

“…The polyphyletism of magnetotaxis and the lack of a clear correlation between genetic clusters and ecology created some confusion in the classification of these organisms that remains partially resolved [17]. Today, we are still unable to state whether or not magnetotactic Magnetospirillum form their own genera [8,18] because their specific ecological boundaries have not been identified yet and they do not form a monophyletic group [8,12]. Current data support the existence of two genetically distinct groups represented by strains MSR-1 and AMB-1 respectively [8].…”

“…Magnetosome biogenesis is encoded by unique genes (referred as the mam and/or mms genes) that are, for most of them, clustered into operons within a specific genomic region [27][28][29]. Compiling studies show both evidence of vertical inheritance of these genes [12,30,31] and multiple acquisitions by horizontal gene transfer (HGT) in some lineages in MTB of the Alphaproteobacteria class [32][33][34] with duplication events [34,35]. These observations raise questions on the evolutionary mechanisms shaping the adaptation to this ecological niche and the phenotypic maintenance at such level of phylogenetic distance between two evolutionarily distinct lineages.…”