Tepidisphaera mucosa gen. nov., sp. nov., a moderately thermophilic member of the class Phycisphaerae in the phylum Planctomycetes, and proposal of a new family, Tepidisphaeraceae fam. nov., and a new order, Tepidisphaerales ord. nov.

Abstract

Three strains of facultatively aerobic, moderately thermophilic bacteria were isolated from terrestrial hot springs in Baikal Lake region and Kamchatka (Russia). Cells of the new isolates were cocci reproducing by binary fission. The temperature range for growth was between 20 and 56 6C and the pH range for growth from pH 4.5 to 8.5, with optimal growth at 47-50 6C and pH 7.0-7.5. The organisms were chemoheterotrophs preferring sugars and polysaccharides as growth substrates. 16S rRNA gene sequences of strains 2842, 2813 and 2918Kr were nearly identical (99.7-100 % similarity) and indicated that the strains belonged to the phylum Planctomycetes. The phylogenetically closest cultivated relatives were Algisphaera agarilytica 06SJR6-2 T and Phycisphaera mikurensis FYK2301M01 T with 16S rRNA gene sequence similarity values of 82.4 and 80.3 %, respectively. The novel strains differed from them by higher growth temperature, sensitivity to NaCl concentration above 3.0 % and by their cellular fatty acids profile. On the basis of phylogenetic and physiological data, strains 2842 T , 2813 and 2918Kr represent a novel genus and species for which we propose the name Tepidisphaera mucosa sp. nov. The type strain is 2842 T (5VKM B-2832. We also propose that Tepidisphaera gen. nov. is the type genus of a novel family, Tepidisphaeraceae fam. nov. and a novel order, Tepidisphaerales ord. nov.Thermophilic micro-organisms represent diverse phylogenetic lineages of prokaryotes, including new deep ones (Cole et al., 2013; Kawaichi et al., 2013;Podosokorskaya et al., 2013). Some phylogenetic groups inhabiting thermal environments contain only thermophiles, while others contain organisms with different temperature characteristics (Lebedinsky et al., 2007). Thermophilic representatives are now found even in bacterial phyla previously considered to contain only mesophilic prokaryotes, such as the phylum Acidobacteria (Losey et al., 2013). Another example is the phylum Planctomycetes. Analysis of the diversity and distribution of this group in thermal environments based on environmental molecular data revealed several phylogenetic groups of the phylum Planctomycetes most frequently detected in these habitats (A. Yu. Merkel and others, unpublished results). Several isolates from different terrestrial and subsurface thermal habitats were obtained, enriched and/or isolated in pure cultures and identified as members of the new genus 'Thermogutta' (Slobodkina et al., 2014) which is part of the Pirellula-Blastopirellula-Rhodopirellula cluster. These organisms, together with a representative of the genus 'Thermopirellula' (name not validly published; Liu et al., 2012), are to our knowledge the first thermophilic representatives of the phylum Planctomycetes.Abbreviation: ECL, equivalent chain length.

High Diversity of Planctomycetes in Soils of Two Lichen-Dominated Sub-Arctic Ecosystems of Northwestern Siberia

“…The first and so far the only characterized representative of this lineage, which is now defined as the class Phycisphaerae and the order Tepidisphaerales (and implemented as such in the recently released Silva 128), was described last year. This is the moderately thermophilic planctomycete from terrestrial hot springs, Tepidisphaera mucosa (Kovaleva et al, 2015). Similar to other described members of the Phycisphaerae, this planctomycete divides by binary fission and is capable of degrading various polysaccharides.…”

“…Yet, most cultured and taxonomically characterized representatives of this phylum are mesophiles (Ward, 2010). Several moderately thermophilic planctomycetes were also described (Giovannoni et al, 1987; Kovaleva et al, 2015; Slobodkina et al, 2015) but psychrophilic members of this phylum are not yet known. At the same time, planctomycetes are commonly detected in various low-temperature ecosystems by molecular surveys.…”

Sugar metabolism of the first thermophilic planctomycete Thermogutta terrifontis: comparative genomic and transcriptomic approaches

“…However, all of these features were reconsidered during the past few years. Their cell walls have been shown to contain a uniquely thin peptidoglycan layer (Jeske et al, 2015), representatives of the novel class Phycisphaerae divide by binary fission (Fukunaga et al, 2009;Kovaleva et al, 2015) instead of budding, and, finally, a few thermophilic and facultative anaerobic representatives were recently isolated (Slobodkina et al, 2015;Kovaleva et al, 2015). Even though no autotrophic planctomycetes were isolated and cultivated so far, members of the third class-level lineage, represented by uncultivated anammox planctomycetes (van de Graaf et al, 1995), are thought to fix CO 2 via the acetyl-CoA pathway (Strous et al, 2006).…”

Harnessing microfluidic streak plate technique to investigate the gut microbiome of Reticulitermes chinensis

“…RNA gene showed 90% similarity to Mailhella massiliensis (Ndongo et al, 2017). The OTU93 recovered in MSP pool represented a member of Acidobacteria, and its 16S RNA gene showed 94% similarity to Vicinamibacter silvestris (Huber et al, 2016); the OTU97 represented an unclassified member of Phycisphaerae and its closest relative is Tepidisphaera mucosa (Kovaleva et al, 2015) (Their 16S rRNA gene similarity is 91%); More interestingly, the OTU98 recovered from MSP pool in this study together with 16S rRNA gene sequences detected in Formosan subterranean termite (Husseneder et al, 2009) and…”

“…The OTU21 represented an unclassified member of Proteobacteria , and its 16S RNA gene showed 90% similarity to Mailhella massiliensis (Ndongo et al., ). The OTU93 recovered in MSP pool represented a member of Acidobacteria , and its 16S RNA gene showed 94% similarity to Vicinamibacter silvestris (Huber et al., ); the OTU97 represented an unclassified member of Phycisphaerae and its closest relative is Tepidisphaera mucosa (Kovaleva et al., ) (Their 16S rRNA gene similarity is 91%); More interestingly, the OTU98 recovered from MSP pool in this study together with 16S rRNA gene sequences detected in Formosan subterranean termite (Husseneder et al., ) and Reticulitermes speratus (Hongoh, Ohkuma, & Kudo, ) clustered to a unique lineage of Verrucomicrobia (Figure e). So far, there is not any bacterial culture showing 16S rRNA gene sequence similarity higher than 80% to this unique lineage.…”