Magnetospirillum sulfuroxidans sp. nov., capable of sulfur-dependent lithoautotrophy and a taxonomic reevaluation of the order Rhodospirillales

The order Rhodospirillales was proposed in 1971 (Pfennig and Truper, 1971), and currently consists of the families Rhodospirillaceae, Acetobacteraceae (Gillis and De Ley, 1986); Geminicoccaceae (Proença et al., 2018); Kiloniellaceae (Wiese et al., 2009); Azospirillaceae, Reyranellaceae, Rhodovibrionaceae, Stellaceae, Terasakiellaceae, Thalassobaculaceae, Thalassospiraceae, and Zavarziniaceae (Hördt et al., 2020). The family Rhodospirillaceae comprises 25 genera that include a broad spectrum of bacterial species with different metabolic properties, such as photoheterotrophy, photoautotrophy, and chemoheterotrophy.

The genus Magnetospirillum was proposed by Schleifer et al. in 1991 (Schleifer et al., 1991) and is currently classified in the family Rhodospirillaceae. Species of the genus Magnetospirillum are best known for their ability to produce intracellular magnetosomes - the membrane-enclosed highly crystalline magnetite mineral (Bazylinski and Frankel, 2004). Magnetosomes are arranged in chains that cause the bacterium to behave like a bar magnet. Magnetosome production is encoded by a so-called magnetosome genomic cluster (MGC) (Uebe and Schüler, 2016). Most previously described Magnetospirillum species were specifically enriched and isolated based on their magnetotactic property (Blakemore et al., 1979, Koziaeva et al., 2019, Schleifer et al., 1991) but the genus also includes several strains lacking magnetosomes (Gorlenko et al., 2011, Shinoda et al., 2005, Thrash et al., 2010). The magnetotactic strains are microaerophilic heterotrophes (Dziuba et al., 2016, Frankel et al., 1979, Koziaeva et al., 2019, Matsunaga et al., 1991, Schleifer et al., 1991), while some also use nitrate as the alternative electron acceptor (Bazylinski and Blakemore, 1983, Matsunaga et al., 1991, Shinoda et al., 2005). Recently, the genus Magnetospirillum was proposed to incorporate a related genus Phaeospirillum (Hördt et al., 2020) which includes anoxygenic purple nonsulfur bacteria lacking magnetosomes (Imhoff et al., 1998). At the same time, Monteil et al. suggested to divide the phenotypically similar Magnetospirillum species into two evolutionarily divergent lineages (Monteil et al., 2020).

This study describes properties of a previously isolated non-magnetotactic representative of the genus Magnetospirillum, strain J10T, capable of lithoautotrophic growth with reduced sulfur compounds in microoxic conditions (Geelhoed et al., 2010, Geelhoed et al., 2009). We propose the species name Magnetospirillum sulfuroxidans sp. nov. for this strain. Furthermore, based on phylogenomic comparison and phenotypic differences, the genus Magnetospirillum is proposed to be reclassified into three genera, including Magnetospirillum, Paramagnetospirillum and Phaeospirillum, while the order Rhiodospirillales is to be amended with several novel families.

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