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Trimethylornithine Membrane Lipids: Discovered in Planctomycetes and Identified in Diverse Environments

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Trimethylornithine Membrane Lipids: Discovered in Planctomycetes and Identified in Diverse Environments H OH metabolites OH Review Trimethylornithine Membrane Lipids: Discovered in Planctomycetes and Identified in Diverse Environments Eli K. Moore Department of Environmental Science, School of Earth and the Environment, Rowan University, Glassboro, NJ 08028, USA; [email protected] Abstract: Intact polar membrane lipids (IPLs) are the building blocks of all cell membranes. There is a wide range of phosphorus-free IPL structures, including amino acid containing IPLs, that can be taxo- nomically specific. Trimethylornithine membrane lipids (TMOs) were discovered in northern wetland Planctomycete species that were isolated and described in the last decade. The trimethylated terminal nitrogen moiety of the ornithine amino acid in the TMO structure gives the lipid a charged polar head group, similar to certain phospholipids. Since their discovery, TMOs have been identified in various other recently described northern latitude Planctomycete species, and in diverse environments including tundra soil, a boreal eutrophic lake, meso-oligotrophic lakes, and hot springs. The majority of environments or enrichment cultures in which TMOs have been observed include predominately heterotrophic microbial communities involved in the degradation of recalcitrant material and/or low oxygen methanogenic conditions at primarily northern latitudes. Other ecosystems occupied with microbial communities that possess similar metabolic pathways, such as tropical peatlands or coastal salt marshes, may include TMO producing Planctomycetes as well, further allowing these lipids to potentially be used to understand microbial community responses to environmental change in a wide range of systems. The occurrence of TMOs in hot springs indicates that these unique lipids could have broad environmental distribution with different specialized functions. Opportunities also exist to investigate the application of TMOs in microbiome studies, including forensic necrobiomes. Further environmental and microbiome lipidomics research involving TMOs will help reveal the Citation: Moore, E.K. evolution, functions, and applications of these unique membrane lipids. Trimethylornithine Membrane Lipids: Discovered in Planctomycetes and Keywords: trimethylornithine; intact polar lipids; cell membrane; Planctomycetes; northern wetlands Identified in Diverse Environments. Metabolites 2021, 11, 49. https:// doi.org/10.3390/metabo11010049 1. Introduction—Amino Acid Containing Membrane Lipids Received: 23 November 2020 Cell membranes are the interface between biological processes and the environment [1]. Accepted: 5 January 2021 Published: 12 January 2021 Intact polar lipids (IPLs) are the constituent components of the cell membrane lipid bilayer, consisting of a polar head group and an apolar core. The diverse molecular structures Publisher’s Note: MDPI stays neu- of IPLs can provide functional and taxonomic information on the microbial community tral with regard to jurisdictional clai- of a given environment [2,3]. Following cell lysis, the head groups of IPLs are rapidly ms in published maps and institutio- cleaved from the core lipids, on the order of days, thus making IPLs representative of living nal affiliations. biomass [4,5]. The structures of IPL head groups are very diverse, including common phosphoglycerol IPLs [6] (e.g., phosphatidylcholine, PC; phosphatidylethanolamine, PE; etc.), and various bacterial IPLs that have polar head groups containing amino acids [7]. The amino acid IPLs phosphatidylserine and homoserine-containing betaine lipids have a Copyright: © 2021 by the author. Li- glycerol backbone, while other amino acid containing lipids are glycerol free. censee MDPI, Basel, Switzerland. Ornithine lipids (OLs) are a common group of glycerol free amino acid containing This article is an open access article lipids in bacteria (Figure1). Approximately 50% of bacteria whose genomes have been distributed under the terms and con- sequenced are predicted to have the capability to synthesize OLs, but the genes necessary ditions of the Creative Commons At- to form OLs are absent in archaea and eukaryotes [7–10]. The OL head group consists of an tribution (CC BY) license (https:// amino acid that is linked by an amide bond to a β-hydroxy fatty acid, and the β-hydroxy creativecommons.org/licenses/by/ 4.0/). fatty acid is “piggy back” esterified to a fatty acid (Figure1). Additionally, lysine containing Metabolites 2021, 11, 49. https://doi.org/10.3390/metabo11010049 https://www.mdpi.com/journal/metabolites Metabolites 2021, 11, x FOR PEER REVIEW 2 of 11 Metabolites 2021, 11, 49 2 of 11 an amino acid that is linked by an amide bond to a β-hydroxy fatty acid, and the β-hy- droxy fatty acid is “piggy back” esterified to a fatty acid (Figure 1). Additionally, lysine containingmembrane membrane lipids synthesized lipids synthesized by Agrobacterium by Agrobacterium tumefaciens tumefaciens[11] and Pedobacter[11] and Pedobacter saltans [12 ] saltanshave [12] the have same the ester same linked ester fatty linked acid fatty moiety acid andmoiety amide and linked amideβ linked-OH-fatty β-OH-fatty acid fatty acid acid fattystructure acid structure that exists that in exists OLs. in OLs. FigureFigure 1. Intact 1. Intact polar polar lipid lipid (IPL) (IPL) structures structures of of orni ornithinethine (OL), (OL), monomethylornithine monomethylornithine (MMO), (MMO), dime- dimethy- thylornithinelornithine (DMO),(DMO), and and trimethylornithine trimethylornithine (TMO) (TMO) lipids lipids including including fatty fatty acid acid and andβ OH-fattyβOH-fatty acid acid core corelipids. lipids. R1 R1 = headgroup;= headgroup; R2, R2, R3 R3 = alkane/alkene = alkane/alkene chains. chains. Ornithine Ornithine (OL; (OL; [13 –[13–15]);15]); monomethylornithine monomethylornithine(MMO; [16]); dimethylornithine (MMO; [16]); (DMO; dimethylorni [16]); trimethylornithinethine (DMO; [16]); (TMO; trimethylornithine [16]). Figure adapted (TMO; from [17]. [16]). Figure adapted from [17]. Ornithine lipids do not contain phosphorus (Figure1), and can be produced by certain bacteriaOrnithine as an lipids alternative do not to phosphoglycerol contain phosphor lipidsus in(Figure response 1), to and phosphorus can be limitationproduced [ 18by,19 ]. certainOrnithine bacteria lipid as head an alternative groups and to the phosphoglycerol fatty acid groups lipids can also in beresponse hydroxylated to phosphorus in response limitationto different [18,19]. environmental Ornithine stress lipid conditionshead groups [20, 21and]. It the has fatty been proposedacid groups that can the hydroxyla-also be hydroxylatedtion of OLs increasesin response hydrogen to different bonding environm betweenental lipid stress molecules, conditions thus [20,21]. providing It has enhanced been proposedmembrane that fluidity the hydroxylation and stability [22 of]. Similarly,OLs increases it was discoveredhydrogen thatbonding lysine lipidsbetween (LLs) lipid can be molecules,hydroxylated thus onproviding both the enhanced head group membrane and fatty acidfluidity chains and in stability response [22]. to temperature Similarly, it and was pH discoveredstress in the that soil lysine bacteria lipidsPedobacter (LLs) can saltans be hy[12droxylated]. While various on both other the microbial head group membrane and fatty lipids acidcan chains be produced in response or modified to temperature in response and to pH changing stress environmentalin the soil bacteria conditions, Pedobacter OLs andsaltans other [12].glycerol-free While various amino other acid lipidsmicrobial are commonly membrane observed lipids can to be be involved produced in stress or modified response in [9 ]. responseIn to 2013, changing three novelenvironmental classes of conditions, amino acid OLs containing and other membrane glycerol-free lipids amino were discov-acid lipidsered are in commonly multiple Planctomycetes observed to bethat involved were isolated in stress from response ombrotrophic [9]. (receives water only fromIn rain)2013, northernthree novel wetlands classes in Europeanof amino northacid Russia:containing mono-, memb di-,rane and lipids trimethylated were discoveredornithine in lipids multiple ([16]; FigurePlanctomycetes1). In particular, that were the isolated unique physicalfrom ombrotrophic properties of(receives trimethy- waterlated only ornithine from lipidsrain) northern (TMOs) appear wetlands to be in adapted European to the north acidic, Russia: low nutrient, mono-, anddi-, anoxicand trimethylatedconditions ofornithine ombrotrophic lipids ([16]; northern Figure wetlands. 1). In particular, Shortly thereafter,the unique TMOs physical were properties identified of trimethylatedin various other ornithine diverse lipids environments (TMOs) appear that are to often be adapted characterized to the acidic, by unique low nutrient, physical or andchemical anoxic conditions conditions. of Thisombrotrophic review will northern summarize wetlands. the discovery Shortly thereafter, of TMOs, TMOs their physical were identifiedand chemical in various properties, other diverse potential environmen functions, andts that distribution are often incharacterized diverse environments. by unique physical or chemical conditions. This review will summarize the discovery of TMOs, their 2. Methylated Ornithine Lipids Discovered in Northern Wetland Planctomycetes physical and chemical properties, potential functions, and distribution in diverse environments.In recent decades, there has been great interest in the changing conditions of Northern peatlands due to warming temperatures
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