Abstract
In paddy soil, bacteria from the family Geobacteraceae have been shown to strongly contribute to the biogeochemical cycle. However, no Geobacteraceae species with validly published names have been isolated from paddy soil. In this study, we isolated and characterized four novel ferric reducing bacteria in the family Geobacteraceae from the paddy soils of three different fields in Japan. The four strains, S43T, Red53T, S62T, and Red111T, were Gram-stain negative, strictly anaerobic, chemoheterotrophic, and motile with peritrichous flagella. Phylogenetic studies based on 16S rRNA gene sequences, five concatenated housekeeping genes (fusA, rpoB, recA, nifD, and gyrB) and 92 concatenated core genes revealed that the four strains belong to the family Geobacteraceae and are most closely related to Geobacter bemidjiensis BemT (97.4–98.2%, 16S rRNA gene sequence similarities) and Geobacter bremensis Dfr1T (97.1–98.0%). Genomic analysis with average nucleotide identity (ANI) and digital DNA–DNA hybridization (GGDC) calculations clearly distinguished the four isolated strains from other species of the family Geobacteraceae and indicated that strains S43T, Red53T, S62T, and Red111T represent independent species, with values below the thresholds for species delineation. Chemotaxonomic characteristics, including major fatty acid and whole cell protein profiles, showed differences among the isolates and their closest relatives, which were consistent with the results of DNA fingerprints and physiological characterization. Additionally, each of the four isolates shared a low 16S rRNA gene sequence similarity (92.4%) and average amino acid identity (AAI) with the type strain of the type species Geobacter metallireducens. Overall, strains S43T, Red53T, S62T, and Red111T represent four novel species, which we propose to classify in a novel genus of the family Geobacteraceae, and the names Geomonas oryzae gen. nov., sp. nov. (type strain S43T), Geomonas edaphica sp. nov. (type strain Red53T), Geomonas ferrireducens sp. nov. (type strain S62T), and Geomonas terrae sp. nov. (type strain Red111T) are proposed. Based on phylogenetic and genomic analyses, we also propose the reclassification of Geobacter bremensis as Geomonas bremensis comb. nov., Geobacter pelophilus as Geomonas pelophila comb. nov., and Geobacter bemidjiensis as Geomonas bemidjiensis comb. nov.
Highlights
The family Geobacteraceae, in the order Desulfuromonadales, class Deltaproteobacteria, was first proposed by Holmes et al (2004) and currently contains a single genus with a validly published name: Geobacter (Garrity et al, 2005; Nevin et al, 2007)
The four microorganisms were isolated from paddy soils collected from different fields in Japan: strains S43T and S62T were isolated from field soil in Nagaoka-shi, Niigata in February
Complete 16S rRNA gene sequences were obtained for strain S43T (1424 bp, accession number MH915553), strain Red53T (1424 bp, accession number MH915554), strain S62T (1424 bp, accession number MH915555), and strain Red111T (1426 bp, accession number MH915556)
Summary
The family Geobacteraceae, in the order Desulfuromonadales, class Deltaproteobacteria, was first proposed by Holmes et al (2004) and currently contains a single genus with a validly published name: Geobacter (Garrity et al, 2005; Nevin et al, 2007). At the time of writing, the family Geobacteraceae contained 19 species with validly published names, which were isolated from different environmental sources, e.g., the type species Geobacter metallireducens GS-15T was isolated from surficial bottom sediment (Lovley et al, 1993), Geobacter daltonii FRC-32T from contaminated sediment (Prakash et al, 2010), Geobacter toluenoxydans TMJ1T from tar-oil-contaminated sludge (Kunapuli et al, 2010), and Geobacter sulfurreducens PCAT from wastewater biofilm (Caccavo et al, 1994) Besides these isolates, dozens of Geobacteraceae clone sequences have been reported from culture-independent analyses in various environments, such as contaminated sediments (Holmes et al, 2009), wastewater (Tejedor-Sanz et al, 2018), paddy soils (Hori et al, 2010; Li et al, 2014), and freshwater lake sediments (Cummings et al, 2003), indicating that the Geobacteraceae family is one of the ubiquitous microbial groups in terrestrial and freshwater ecosystems. Because of these versatile features, Geobacteraceae are important microbes in the biodegradation and bioremediation of environmental pollutants and bioenergy production (Shelobolina et al, 2008; Mouser et al, 2009)
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