Gemmatirosa kalamazoonesis gen. nov., sp. nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes

DeBruyn, Jennifer M.; Fawaz, Mariam N.; Peacock, Aaron D.; Dunlap, John R.; Nixon, Lauren T.; Cooper, Katherine E.; Radosevich, Mark

doi:10.2323/jgam.59.305

Cited by 62 publications

(50 citation statements)

References 20 publications

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“…Capsules and endospores were not observed after staining the cells with Indian ink and malachite green, respectively. Intracellular polyphosphate accumulation was suggested by DAPI (4,6-diamidino-2-phenylindole) staining (DeBruyn et al, 2013;Zhang et al, 2003) and by the presence of electron-dense inclusion bodies in transmission electron micrographs (Fig. 1).…”

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confidence: 98%

“…Gemmatimonas aurantiaca T-27 T was isolated from a laboratory-scale anaerobic-aerobic sequential batch reactor operated under excess biological phosphorus removal , whereas Gemmatimonas phototrophica AP64 T , a microaerophilic, bacteriochlorophyll a-containing bacterium, was isolated from a freshwater lake (Zeng et al, 2015). The genus 'Gemmatirosa' comprises a single species, 'Gemmatirosa kalamazoonensis', of which the proposed type strain KBS708 was isolated from an organically managed agricultural soil (DeBruyn et al, 2013). However, the names of the genus and species…”

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confidence: 99%

“…To test bacterial growth under microaerobic and anaerobic atmospheres, bacterial cultures were incubated on solid R2A noble agar at 25 8C for 30 days. Gemmatimonas aurantiaca and 'Gemmatirosa kalamazoonensis' are also chemo-organoheterotrophic bacteria, but the former grew optimally under aerobic conditions , like strain CB-286315 T , whereas the latter preferred micro-oxic conditions (DeBruyn et al, 2013). Gemmatimonas phototrophica is a microaerophilic, bacteriochlorophyll a-containing bacterium with a facultatively photoheterotrophic metabolism.…”

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confidence: 99%

“…dReported as 20-40 8C (optimum 37 8C) by DeBruyn et al (2013). §Reported as pH 6.0-10.0 (optimum pH 7.0-7.5) by Zeng et al (2015).…”

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Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers

Pascual

García-López

Bills

et al. 2016

International Journal of Systematic and Evolutionary Microbiology

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Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers A novel chemo-organoheterotroph bacterium, strain CB-286315 T , was isolated from a Mediterranean forest soil sampled at the Sierra de Tejeda, Almijara and Alhama Natural Park, Spain, by using the diffusion sandwich system, a device with 384 miniature diffusion chambers. 16S rRNA gene sequence analyses identified the isolate as a member of the under-represented phylum Gemmatimonadetes, where 'Gemmatirosa kalamazoonensis' KBS708, Gemmatimonas aurantiaca T-27 T and Gemmatimonas phototrophica AP64 T were the closest relatives, with respective similarities of 84.4, 83.6 and 83.3 %. Strain CB-286315 T was characterized as a Gram-negative, non-motile, short to long rod-shaped bacterium. Occasionally, some cells attained an unusual length, up to 35-40 mm. The strain showed positive responses for catalase and cytochrome-c oxidase and division by binary fission, and exhibited an aerobic metabolism, showing optimal growth under normal atmospheric conditions. Strain CB-286315 T was also able to grow under micro-oxic atmospheres, but not under anoxic conditions. The strain is a slowly growing bacterium able to grow under low nutrient concentrations. Major fatty acids included iso-C 17 : 1 v9c, summed feature 3 (C 16 : 1 v7c and/or iso-C 15 : 0 2-OH), C 16 : 0 and iso-C 17 : 0 . The major polar lipids were phosphatidylglycerol, phosphatidylethanolamine, phosphatidylcholine, two unidentified glycolipids and three phospholipids. The major isoprenoid quinone was MK-8 and the diagnostic diamino acid was meso-diaminopimelic acid. The DNA G+C content was 67.0 mol%. Based on a polyphasic taxonomic characterization, strain CB-286315 T represents a novel genus and species, Longimicrobium terrae gen. nov., sp. nov., within the phylum Gemmatimonadetes. The type strain of Longimicrobium terrae is strain CB-286315 T ( 5 DSM 29007 T 5 CECT 8660 T ). In order to classify the novel taxon within the existing taxonomic framework, the family Longimicrobiaceae fam. nov., order Longimicrobiales ord. nov. and class Longimicrobia classis nov. are also proposed.The phylum Gemmatimonadetes is a cosmopolitan bacterial taxon, members of which inhabit a wide variety of ecological niches (DeBruyn et al., 2011;Hanada & Sekiguchi, 2014;Zhang et al., 2003) including terrestrial and marine environments (Kamagata, 2010). Although they are found worldwide, members of the phylum are usually found at low frequency in soil microbial communities, with relative abundances ranging from 0.2 to 6.5 % (DeBruyn et al., 2011). Presently, .13 000 environmental 16S rRNA gene sequences available in the SILVA SSU Ref 123 database are likely to be associated with the phylum Gemmatimonadetes (Quast et al., 2013). According to the environmental 16S rRNA gene sequences, the phylum Gemmatimonadetes can be divided into five major lineages at the class level (groups 1-5) (Hanada & Sekiguchi, 2014). Group ...

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confidence: 98%

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confidence: 99%

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confidence: 99%

“…dReported as 20-40 8C (optimum 37 8C) by DeBruyn et al (2013). §Reported as pH 6.0-10.0 (optimum pH 7.0-7.5) by Zeng et al (2015).…”

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confidence: 99%

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Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers

Pascual

García-López

Bills

et al. 2016

International Journal of Systematic and Evolutionary Microbiology

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“…Gemmatimonadetes have been identified as one of the most abundant phyla of bacteria in soil environments and often constitute Ͼ2% of the total bacterial population (23,24); however, only three representative strains of this phylum (Gemmatimonas aurantiaca strain T-27, Gemmatirosa kalamazoonesis strain KBS708, and Gemmatimonas phototrophica strain AP64) have been isolated to date, and the physiological characteristics of these organisms are virtually unknown (25)(26)(27)(28). Although clade II nosZ genes were found in the genomes of G. aurantiaca strain T-27 and G. kalamazoonesis strain KBS708, these strains were both characterized as obligate aerobes, and respiration on any other electron acceptors, e.g., N 2 O, has yet to be explored (25)(26)(27). Therefore, questions remain unanswered regarding the functionality of this Gemmatimonadetes NosZ and its potential physiological role as a respiratory enzyme.…”

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Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

Park

Kim

Yoon

2017

Appl Environ Microbiol

128

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N 2 O-reducing organisms with nitrous oxide reductases (NosZ) are known as the only biological sink of N 2 O in the environment. Among the most abundant nosZ genes found in the environment are nosZ genes affiliated with the understudied Gemmatimonadetes phylum. In this study, a unique regulatory mechanism of N 2 O reduction in Gemmatimonas aurantiaca strain T-27, an isolate affiliated with the Gemmatimonadetes phylum, was examined. Strain T-27 was incubated with N 2 O and/or O 2 as the electron acceptor. Significant N 2 O reduction was observed only when O 2 was initially present. When batch cultures of strain T-27 were amended with O 2 and N 2 O, N 2 O reduction commenced after O 2 was depleted. In a long-term incubation with the addition of N 2 O upon depletion, the N 2 O reduction rate decreased over time and came to an eventual stop. Spiking of the culture with O 2 resulted in the resuscitation of N 2 O reduction activity, supporting the hypothesis that N 2 O reduction by strain T-27 required the transient presence of O 2 . The highest level of nosZ transcription (8.97 nosZ transcripts/recA transcript) was observed immediately after O 2 depletion, and transcription decreased ϳ25-fold within 85 h, supporting the observed phenotype. The observed difference between responses of strain T-27 cultures amended with and without N 2 O to O 2 starvation suggested that N 2 O helped sustain the viability of strain T-27 during temporary anoxia, although N 2 O reduction was not coupled to growth. The findings in this study suggest that obligate aerobic microorganisms with nosZ genes may utilize N 2 O as a temporary surrogate for O 2 to survive periodic anoxia.IMPORTANCE Emission of N 2 O, a potent greenhouse gas and ozone depletion agent, from the soil environment is largely determined by microbial sources and sinks. N 2 O reduction by organisms with N 2 O reductases (NosZ) is the only known biological sink of N 2 O at environmentally relevant concentrations (up to ϳ1,000 parts per million by volume [ppmv]). Although a large fraction of nosZ genes recovered from soil is affiliated with nosZ found in the genomes of the obligate aerobic phylum Gemmatimonadetes, N 2 O reduction has not yet been confirmed in any of these organisms. This study demonstrates that N 2 O is reduced by an obligate aerobic bacterium, Gemmatimonas aurantiaca strain T-27, and suggests a novel regulation mechanism for N 2 O reduction in this organism, which may also be applicable to other obligate aerobic organisms possessing nosZ genes. We expect that these findings will significantly advance the understanding of N 2 O dynamics in environments with frequent transitions between oxic and anoxic conditions.

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L ongimicrobiaceae

Pascual¹,

Genilloud²

2018

Bergey's Manual of Systematics of Archaea and Bacteria

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Lon.gi.mi.cro.bi.a.ce'ae. N.L. neut. n. Longimicrobium type genus of the family; suff. ‐ aceae ending to denote a family; N.L. neut. pl. n. Longimicrobiaceae the Longimicrobium family. Gemmatimonadetes / Longimicrobia / Longimicrobiales / Longimicrobiaceae The Longimicrobiaceae are delineated from other taxa based on 16S rRNA gene analysis. The family is a member of the order Longimicrobiales within the class Longimicrobia (formerly group 3 of the taxonomic scheme proposed by Hanada and Sekiguchi, 2014). Gram‐negative, nonmotile, short to long rod‐shaped bacteria with an aerobic chemoorganoheterotrophic metabolism. Mesophilic, neutrophilic or slightly alkaliphilic, and nonhalophilic bacteria. The major fatty acids are iso‐C 17:1 ω9 c , summed feature 3 (C 16:1 ω7 c and/or iso‐C 15:0 2‐OH), C 16:0 , and iso‐C 17:0 . Major polar lipids are phosphatidylglycerol, phosphatidylethanolamine, phosphatidylcholine, two unidentified glycolipids, and three phospholipids. The major isoprenoid quinone is MK‐8. The diagnostic diamino acid is meso‐diaminopimelic acid. The sole cultured representative of the family so far is the type strain of Longimicrobium terrae . DNA G + C content (mol%) : 67.0 (HPLC). Type genus : Longimicrobium Pascual, García‐López, Bills and Genilloud 2016, 1982 VP .

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Gemmatirosa kalamazoonesis gen. nov., sp. nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes

Cited by 62 publications

References 20 publications

Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers

Longimicrobium terrae gen. nov., sp. nov., an oligotrophic bacterium of the under-represented phylum Gemmatimonadetes isolated through a system of miniaturized diffusion chambers

Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

L ongimicrobiaceae

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