Abstract:Pyrinomonas methylaliphatogenes gen. nov., sp. nov., a novel group 4 thermophilic member of the phylum Acidobacteria from geothermal soils An aerobic, thermophilic, moderately acidophilic non-spore-forming bacterium, strain K22 T , was isolated from geothermally heated soil at Mount Ngauruhoe, New Zealand. On the basis of 16S rRNA gene sequence similarity, K22 T was shown to belong to subdivision 4 of the phylum Acidobacteria and to be most closely related to 'Candidatus Chloracidobacterium thermophilum' (86 %… Show more
“…Seven strains of bacteria belonging to Acidobacteria SD 4 were analyzed for their lipid compositions; five are species that have previously been characterized (Blastocatella fastidiosa [42], Pyrinomonas methylaliphatogenes [44], "Ca. Chloracidobacterium thermophilum" [41], Aridibacter famidurans, and Aridibacter kavangonensis [43]), and two are novel strains isolated from soils in Namibia (Table 1).…”
Section: Resultsmentioning
confidence: 99%
“…Blastocatella fastidosa, an aerobic chemoorganoheterotroph (42), and two Aridibacter species (43) were isolated from semiarid savannah soils. The thermophile Pyrinomonas methylaliphatogenes was isolated from a geothermally heated soil and possesses a chemoheterotrophic and obligately aerobic metabolism (44). Molecular ecological studies based on 16S rRNA genes have indicated that, in wetlands, the most abundant Acidobacteria members fall in SD 1 and 3 (21), whereas in lakes SD 1, 6, and 7 thrive (45).…”
e Recently, iso-diabolic acid (13,16-dimethyl octacosanedioic acid) has been identified as a major membrane-spanning lipid of subdivisions 1 and 3 of the Acidobacteria, a highly diverse phylum within the Bacteria. This finding pointed to the Acidobacteria as a potential source for the bacterial glycerol dialkyl glycerol tetraethers that occur ubiquitously in peat, soil, lakes, and hot springs. Here, we examined the lipid composition of seven phylogenetically divergent strains of subdivision 4 of the Acidobacteria, a bacterial group that is commonly encountered in soil. Acid hydrolysis of total cell material released iso-diabolic acid derivatives in substantial quantities (11 to 48% of all fatty acids). In contrast to subdivisions 1 and 3 of the Acidobacteria, 6 out of the 7 species of subdivision 4 (excepting "Candidatus Chloracidobacterium thermophilum") contained iso-diabolic acid ether bound to a glycerol in larger fractional abundance than iso-diabolic acid itself. This is in agreement with the analysis of intact polar lipids (IPLs) by high-performance liquid chromatography-mass spectrometry (HPLC-MS), which showed the dominance of mixed ether-ester glycerides. iso-Diabolic acid-containing IPLs were not identified, because these IPLs are not released with a Bligh-Dyer extraction, as observed before when studying lipid compositions of subdivisions 1 and 3 of the Acidobacteria. The presence of ether bonds in the membrane lipids does not seem to be an adaptation to temperature, because the five mesophilic isolates contained a larger amount of ether lipids than the thermophile "Ca. Chloracidobacterium thermophilum." Furthermore, experiments with Pyrinomonas methylaliphatogenes did not reveal a major influence of growth temperature over the 50 to 69°C range.
“…Seven strains of bacteria belonging to Acidobacteria SD 4 were analyzed for their lipid compositions; five are species that have previously been characterized (Blastocatella fastidiosa [42], Pyrinomonas methylaliphatogenes [44], "Ca. Chloracidobacterium thermophilum" [41], Aridibacter famidurans, and Aridibacter kavangonensis [43]), and two are novel strains isolated from soils in Namibia (Table 1).…”
Section: Resultsmentioning
confidence: 99%
“…Blastocatella fastidosa, an aerobic chemoorganoheterotroph (42), and two Aridibacter species (43) were isolated from semiarid savannah soils. The thermophile Pyrinomonas methylaliphatogenes was isolated from a geothermally heated soil and possesses a chemoheterotrophic and obligately aerobic metabolism (44). Molecular ecological studies based on 16S rRNA genes have indicated that, in wetlands, the most abundant Acidobacteria members fall in SD 1 and 3 (21), whereas in lakes SD 1, 6, and 7 thrive (45).…”
e Recently, iso-diabolic acid (13,16-dimethyl octacosanedioic acid) has been identified as a major membrane-spanning lipid of subdivisions 1 and 3 of the Acidobacteria, a highly diverse phylum within the Bacteria. This finding pointed to the Acidobacteria as a potential source for the bacterial glycerol dialkyl glycerol tetraethers that occur ubiquitously in peat, soil, lakes, and hot springs. Here, we examined the lipid composition of seven phylogenetically divergent strains of subdivision 4 of the Acidobacteria, a bacterial group that is commonly encountered in soil. Acid hydrolysis of total cell material released iso-diabolic acid derivatives in substantial quantities (11 to 48% of all fatty acids). In contrast to subdivisions 1 and 3 of the Acidobacteria, 6 out of the 7 species of subdivision 4 (excepting "Candidatus Chloracidobacterium thermophilum") contained iso-diabolic acid ether bound to a glycerol in larger fractional abundance than iso-diabolic acid itself. This is in agreement with the analysis of intact polar lipids (IPLs) by high-performance liquid chromatography-mass spectrometry (HPLC-MS), which showed the dominance of mixed ether-ester glycerides. iso-Diabolic acid-containing IPLs were not identified, because these IPLs are not released with a Bligh-Dyer extraction, as observed before when studying lipid compositions of subdivisions 1 and 3 of the Acidobacteria. The presence of ether bonds in the membrane lipids does not seem to be an adaptation to temperature, because the five mesophilic isolates contained a larger amount of ether lipids than the thermophile "Ca. Chloracidobacterium thermophilum." Furthermore, experiments with Pyrinomonas methylaliphatogenes did not reveal a major influence of growth temperature over the 50 to 69°C range.
“…The abundance of transporters specific for amino acids, polyamines and organocations seemed to be especially high in the genomes stemming from terrestrial strains (Supporting Information Table S6), suggesting their potential to not only use inorganic but also organic N sources via mineralization. Soils have been reported to contain varying types and amounts of free amino acids (Monreal and McGill, 1985;Kielland, 1994), which could serve as a source of N. Although select strains have been reported to grow on ammonia, nitrate, nitrite and/or amino acids (Eichorst, 2007;Koch et al, 2008;Dedysh et al, 2012;Crowe et al, 2014;Tank and Bryant, 2015b;Myers and King, 2016;Vieira et al, 2017;D. Trojan and S.A. Eichorst, unpublished data), a more detailed growth-based study is warranted, as previous work illustrated that while C. thermophilum B harboured putative genes for ammonium uptake, it was unable to grow solely on ammonium (Tank and Bryant, 2015b).…”
Section: Assimilatory Nitrogen Metabolism Nitrification and Nitrogenmentioning
confidence: 99%
“…Based on previous genomic and physiological investigations, many subdivision 1 and 3 strains have been described as versatile heterotrophs that grow optimally at low pH, produce copious amounts of extracellular material, harbour a low rRNA operon copy number suggesting an oligotrophic (more K-selected) lifestyle, and contain both low-specificity major facilitator superfamily and high-affinity ABC-type transporters (Ward et al, 2009;Rawat et al, 2012;Kielak et al, 2016). Some more striking physiologies such as iron reduction and/or fermentative growth (Liesack et al, 1994;Coates et al, 1999), phototrophy (Garcia Costas et al, 2012), along with the ability to grow under thermophilic conditions have been described in select strains from subdivision 4, 8, 10 and 23 (Izumi et al, 2012;Losey et al, 2013;Crowe et al, 2014;Stamps et al, 2014;Tank and Bryant, 2015a). Yet the vast majority of acidobacteria detected in soils based on culture dependent and independent approaches are members of subdivisions 1, 2, 3, 4, 5 and 6 (Janssen, 2006;Jones et al, 2009).…”
Section: Introductionmentioning
confidence: 99%
“…o. Tank and Bryant (2015a,b); p Crowe et al, 2014;. q. Vieira et al, 2017; r. Liesack et al, 1994; s. Coates et al, 1999; t. Losey et al, 2013.…”
SummaryMembers of the phylum Acidobacteria are abundant and ubiquitous across soils. We performed a large‐scale comparative genome analysis spanning subdivisions 1, 3, 4, 6, 8 and 23 (n = 24) with the goal to identify features to help explain their prevalence in soils and understand their ecophysiology. Our analysis revealed that bacteriophage integration events along with transposable and mobile elements influenced the structure and plasticity of these genomes. Low‐ and high‐affinity respiratory oxygen reductases were detected in multiple genomes, suggesting the capacity for growing across different oxygen gradients. Among many genomes, the capacity to use a diverse collection of carbohydrates, as well as inorganic and organic nitrogen sources (such as via extracellular peptidases), was detected – both advantageous traits in environments with fluctuating nutrient environments. We also identified multiple soil acidobacteria with the potential to scavenge atmospheric concentrations of H2, now encompassing mesophilic soil strains within the subdivision 1 and 3, in addition to a previously identified thermophilic strain in subdivision 4. This large‐scale acidobacteria genome analysis reveal traits that provide genomic, physiological and metabolic versatility, presumably allowing flexibility and versatility in the challenging and fluctuating soil environment.
Py.ri.no.mo.na.da.ce'ae. N.L. fem. n.
Pyrinomonas
, type genus of the family; suff.
‐aceae
ending to denote a family; N.L. fem. pl. n.
Pyrinomonadaceae
, the
Pyrinomonas
family.
Acidobacteria / Blastocatellia / Blastocatellales / Pyrinomonadaceae
The
Pyrinomonadaceae
are delineated from other taxa based on 16S rRNA gene analysis. The family is a member of the order
Blastocatellales
within the class
Blastocatellia
(formerly: subdivision 4
Acidobacteria
). Cells are ovoid or rod shaped, divide by binary fission, and stain Gram‐negative. Cells are nonmotile and form neither spores nor capsules. Aerobic chemoorganoheterotrophs, unable to grow phototrophically, and unable to reduce nitrate or ferment glucose. Cytochrome
c
oxidase and catalase activities are variable. Mesophiles or thermophiles, which are adapted to a broad range of pH values.
Pyrinomonadaceae
utilize a limited number of growth substrates with a preference for complex proteinaceous compounds. The ability to hydrolyze polymers is variable among species. All genera of the
Pyrinomonadaceae
contain phosphatidylethanolamine and MK‐8 as major polar lipid and respiratory quinone, respectively. Some representatives also contain minor amounts of MK‐7. Iso‐C
15
:0
is the major fatty acid. Other major fatty acids are variable among the genera. After direct acid hydrolysis of biomass, 13,16‐dimethyl octacosanedioic acid (iso‐diabolic acid) and its monoalkyl glycerol ether derivatives are detected in all members tested to date. The DNA G + C content ranges from 54.7 to 66.9 mol%. Members of the family
Pyrinomonadaceae
have been isolated from semiarid savannah and volcanic soils.
DNA G
+
C content (mol%)
: 54.7–66.9.
Type genus
:
Pyrinomonas
Crowe, Power, Morgan, Dunfield, Lagutin, Rijpstra, Vyssotski, Sinninghe Damsté, Houghton, Ryan, and Stott 2014, 225
VP
.
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