OlsG (Sinac_1600) Is an Ornithine Lipid N-Methyltransferase from the Planctomycete Singulisphaera acidiphila

Escobedo‐Hinojosa, Wendy; Vences‐Guzmán, Miguel Ángel; Schubotz, Florence; Sandoval-Calderón, Mario; Summons, Roger E.; López‐Lara, Isabel M.; Geiger, Otto; Sohlenkamp, Christian

doi:10.1074/jbc.m115.639575

Cited by 20 publications

(24 citation statements)

References 41 publications

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“…TMOs were recently described for the first time in four isolated Planctomycetes from ombrotrophic wetlands from north Russia (Moore et al ), while the gene involved in the methylation of the ornithine lipid head group to form TMOs has also been found in the Gammaproteobacteria Arhodomonas aquaeolei (Escobedo‐Hinojosa et al ). Moore et al () postulated that the methylation of ornithines may be an adaption by the Planctomycetes to increase their membrane stability under acidic conditions without using P, which is scarce in ombrotrophic conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Ornithine and TMO lipids are exclusively associated with bacteria (L opez-Lara et al 2003;Moore et al 2013;Escobedo-Hinojosa et al 2015) and around 50% of all bacteria have the genetic capacity to synthesize ornithines (Vences-Guzm an et al 2015). The higher relative percentage of ornithine and TMO lipids in oligo-mesotrophic lakes may thus indicate a higher amount of bacterial biomass relative to phytoplankton biomass than in the more eutrophic lakes.…”

Section: Influence Of Trophic State On Ipl Distributionmentioning

confidence: 99%

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Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Bale

Hopmans

Schoon

et al. 2016

Limnology & Oceanography

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We characterized the intact polar lipid (IPL) composition in the surface waters of 22 lakes from Minnesota and Iowa, ranging in trophic state between eutrophic and oligo-mesotrophic, to investigate the impact of trophic state on IPL composition. A high diversity of IPL classes was detected. Most IPL classes were detected in all lakes, but the eutrophic lakes contained a significantly higher relative abundance of lysophosphatidylcholine (PC) than the oligo-mesotrophic lakes, which in turn were characterized by significantly higher relative abundance of hydroxymethyltrimethyl-alanine/trimethyl-homoserine (DGTA/DGTS) betaines, ornithine lipids and the recently discovered trimethyl ornithine (TMO) lipids. The higher relative abundance of ornithines and TMOs may relate to a higher contribution of heterotrophic bacteria relative to phytoplankton while the higher abundance of the DGTA/DGTS betaines may relate to substitution by microorganisms of these non-P lipids for PC under P-stress, as has been observed in other environments. We also detected a variety of heterocyst glycolipids (HGs) derived from N 2 -fixing heterocystous Cyanobacteria in all lakes, suggesting the presence of these Cyanobacteria in the full range of trophic conditions. Correlation of HG abundance with environmental data showed that high productivity lakes have high HG abundances, while other distributional differences in HGs, which did not correlate with environmental parameters, are likely due to differences in species composition. We conclude that the significant differences in IPL composition between the eutrophic and oligo-mesotrophic lakes are either due to adaptation of the membrane composition to nutrient conditions or due to general divergences in microbial composition under the different conditions.

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Section: Discussionmentioning

confidence: 99%

Section: Influence Of Trophic State On Ipl Distributionmentioning

confidence: 99%

Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Bale

Hopmans

Schoon

et al. 2016

Limnology & Oceanography

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“…In certain bacteria, OLs can be produced in response to phosphorus limitation (65,66) or modified in response to temperature or acid stress (67)(68)(69). TMOs are essentially modified OLs (38,70); the addition of three methyl groups to the terminal nitrogen of TMOs results in a quaternary amine functional group, which is positively charged, making the lipid more polar and giving it a more cylindrical shape than conically shaped OLs, as observed in the methylation of conical PEs to yield cylindrical polar PCs. The increased relative abundance of TMOs compared to PCs and PGs and the increased relative abundance of TMOs with C 19:1 and ␤OH-C 18:0 fatty acids in PX4 strain cultures under micro-oxic growth conditions (Fig.…”

Section: Discussionmentioning

confidence: 99%

Abundant Trimethylornithine Lipids and Specific Gene Sequences Are Indicative of Planctomycete Importance at the Oxic/Anoxic Interface in Sphagnum-Dominated Northern Wetlands

Moore

Villanueva

Hopmans

et al. 2015

Appl Environ Microbiol

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cNorthern wetlands make up a substantial terrestrial carbon sink and are often dominated by decay-resistant Sphagnum mosses. Recent studies have shown that planctomycetes appear to be involved in degradation of Sphagnum-derived debris. Novel trimethylornithine (TMO) lipids have recently been characterized as abundant lipids in various Sphagnum wetland planctomycete isolates, but their occurrence in the environment has not yet been confirmed. We applied a combined intact polar lipid (IPL) and molecular analysis of peat cores collected from two northern wetlands (Saxnäs Mosse [Sweden] and Obukhovskoye [Russia]) in order to investigate the preferred niche and abundance of TMO-producing planctomycetes. TMOs were present throughout the profiles of Sphagnum bogs, but their concentration peaked at the oxic/anoxic interface, which coincided with a maximum abundance of planctomycete-specific 16S rRNA gene sequences. The sequences detected at the oxic/anoxic interface were affiliated with the Isosphaera group, while sequences present in the anoxic peat layers were related to an uncultured planctomycete group. Pyrosequencing-based analysis identified Planctomycetes as the major bacterial group at the oxic/anoxic interface at the Obukhovskoye peat (54% of total 16S rRNA gene sequence reads), followed by Acidobacteria (19% reads), while in the Saxnäs Mosse peat, Acidobacteria were dominant (46%), and Planctomycetes contributed to 6% of the total reads. The detection of abundant TMO lipids in planctomycetes isolated from peat bogs and the lack of TMO production by cultures of acidobacteria suggest that planctomycetes are the producers of TMOs in peat bogs. The higher accumulation of TMOs at the oxic/anoxic interface and the change in the planctomycete community with depth suggest that these IPLs could be synthesized as a response to changing redox conditions at the oxic/anoxic interface. P eat-accumulating northern wetlands are important sinks for terrestrial carbon, making up one-third of the global soil organic carbon pool (1-4). Nutrient-poor and acidic conditions, as well as low temperatures and decay-resistant Sphagnum mossdominated vegetation, result in low rates of microbial decomposition of plant debris and net carbon sequestration in these ecosystems (5-12). However, carbon respiration has been shown to accelerate in subsurface peat due to climate warming in the subarctic (13) and in simulations of climate warming (14). Additionally, the decomposition of organic matter in anoxic peat layers of northern wetlands is also a significant source of methane in the atmosphere (15-18). Permafrost melt has been shown to result in a net carbon release in northern tundra, including methane emission from thaw lakes (19)(20)(21)(22). The microbial community responsible for decomposition of Sphagnum-derived litter is unique compared to other soil systems and is important to the global carbon cycle (23)(24)(25). Further study on the physiology of this microbial community is needed to understand how it will respond to changing enviro...

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“…Recently, the gene encoding the key enzyme for synthesis of N-methylated phosphorus-free ornithine membrane lipids, N-methyltransferase (OlsG), was identified in the genome of Singulisphaera acidiphila DSM 18658 T (Sinac_1600) (24) and later detected in genomes of other members of the family Isosphaeraceae (11). Our analysis revealed that distant homologs of Sinac_1600 are also present in the genomes of Gemmataceae planctomycetes, including F. ruber SP5 T , Zavarzinella formosa A10 T , and Gemmata sp.…”

Section: Chitin As a Source Of C Chitin As A Source Of Nmentioning

confidence: 99%

Genome Analysis of Fimbriiglobus ruber SP5^T, a Planctomycete with Confirmed Chitinolytic Capability

Ravin

Rakitin

Ivanova

et al. 2018

Appl Environ Microbiol

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Members of the bacterial order have often been observed in associations with Crustacea. The ability to degrade chitin, however, has never been reported for any of the cultured planctomycetes although utilization of-acetylglucosamine (GlcNAc) as a sole carbon and nitrogen source is well recognized for these bacteria. Here, we demonstrate the chitinolytic capability of a member of the family , SP5, which was isolated from a peat bog. As revealed by metatranscriptomic analysis of chitin-amended peat, the pool of 16S rRNA reads from increased in response to chitin availability. Strain SP5 displayed only weak growth on amorphous chitin as a sole source of carbon but grew well with chitin as a source of nitrogen. The genome of SP5 is 12.364 Mb in size and is the largest among all currently determined planctomycete genomes. It encodes several enzymes putatively involved in chitin degradation, including two chitinases affiliated with the glycoside hydrolase (GH) family GH18, GH20 family β--acetylglucosaminidase, and the complete set of enzymes required for utilization of GlcNAc. The gene encoding one of the predicted chitinases was expressed in , and the endochitinase activity of the recombinant enzyme was confirmed. The genome also contains genes required for the assembly of type IV pili, which may be used to adhere to chitin and possibly other biopolymers. The ability to use chitin as a source of nitrogen is of special importance for planctomycetes that inhabit N-depleted ombrotrophic wetlands. Planctomycetes represent an important part of the microbial community in -dominated peatlands, but their potential functions in these ecosystems remain poorly understood. This study reports the presence of chitinolytic potential in one of the recently described peat-inhabiting members of the family, SP5 This planctomycete uses chitin, a major constituent of fungal cell walls and exoskeletons of peat-inhabiting arthropods, as a source of nitrogen in N-depleted ombrotrophic -dominated peatlands. This study reports the chitin-degrading capability of representatives of the order.

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OlsG (Sinac_1600) Is an Ornithine Lipid N-Methyltransferase from the Planctomycete Singulisphaera acidiphila

Cited by 20 publications

References 41 publications

Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Abundant Trimethylornithine Lipids and Specific Gene Sequences Are Indicative of Planctomycete Importance at the Oxic/Anoxic Interface in Sphagnum-Dominated Northern Wetlands

Genome Analysis of Fimbriiglobus ruber SP5^T, a Planctomycete with Confirmed Chitinolytic Capability

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OlsG (Sinac_1600) Is an Ornithine Lipid N-Methyltransferase from the Planctomycete Singulisphaera acidiphila

Cited by 20 publications

References 41 publications

Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Impact of trophic state on the distribution of intact polar lipids in surface waters of lakes

Abundant Trimethylornithine Lipids and Specific Gene Sequences Are Indicative of Planctomycete Importance at the Oxic/Anoxic Interface in Sphagnum-Dominated Northern Wetlands

Genome Analysis of Fimbriiglobus ruber SP5T, a Planctomycete with Confirmed Chitinolytic Capability

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Genome Analysis of Fimbriiglobus ruber SP5^T, a Planctomycete with Confirmed Chitinolytic Capability