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Lipidomics for Geochemistry This article was originally published in Treatise on Geochemistry, Second Edition published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Pearson A. (2014) Lipidomics for Geochemistry. In: Holland H.D. and Turekian K.K. (eds.) Treatise on Geochemistry, Second Edition, vol. 12, pp. 291-336. Oxford: Elsevier. © 2014 Elsevier Ltd. All rights reserved. Author's personal copy 12.11 Lipidomics for Geochemistry A Pearson, Harvard University, Cambridge, MA, USA ã 2014 Elsevier Ltd. All rights reserved. 12.11.1 Introduction 291 12.11.2 Lipid Biosynthetic Pathways 292 12.11.2.1 Acetogenic Lipids 292 12.11.2.2 Isoprenoids – MVA Pathway 295 12.11.2.3 Isoprenoids – MEP Pathway 296 12.11.2.4 Ether and Ester Linkages to Glycerol – Bacteria and Eukaryotes 297 12.11.2.5 Diethers and Tetraethers of Archaea 300 12.11.2.6 Glycerol Membrane Lipids: Final Comments 302 12.11.2.7 Polar Head Groups 302 12.11.2.8 Linear Polyprenes 308 12.11.2.9 Hopanoids 308 12.11.2.10 Steroids 309 12.11.2.11 Ladderanes 310 12.11.2.12 Long-Chain Alkenones 312 12.11.2.13 Highly Branched Isoprenoids of Diatoms 312 12.11.3 Case Studies and Approaches to Lipidomics 313 12.11.3.1 Examples Using Bacterial Genetics 314 12.11.3.1.1 Role of squalene–hopene cyclase in the synthesis of hopanoid lipids 315 12.11.3.1.2 Synthesis of A-ring methylated bacteriohopanepolyols 316 12.11.3.1.3 Synthesis of hopanoid C5 side chains 317 12.11.3.2 Examples Using Genomic Data from Characterized Species 317 12.11.3.2.1 Bacteria capable of sterol biosynthesis 318 12.11.3.2.2 Anaerobes capable of synthesizing hopanoids 318 12.11.3.2.3 The distribution of phosphatidylcholine in bacteria 319 12.11.3.2.4 Hypotheses about synthesis of ladderane lipids 319 12.11.3.3 Examples Using Environmental Metagenomics and Functional Genomics 320 12.11.3.3.1 Functional gene surveys – environmental shc genes 320 12.11.3.3.2 General metagenomic surveys – hopanoid synthesis genes 321 12.11.3.3.3 General metagenomic surveys – other lipid biosynthetic pathways 322 12.11.3.4 Examples Using Experimental Biochemical Approaches 324 12.11.3.4.1 Synthesis of botryococcene 324 12.11.3.4.2 Multifunctional 2,3-oxidosqualene cyclases in plants 324 12.11.3.5 Examples Using SSU rRNA Combined with Taxonomic Specificity of Algal Biomarkers 325 12.11.3.5.1 Paleorecord of alkenone-producing haptophyte algae 326 12.11.3.5.2 Highly branched isoprenoids of diatoms 326 12.11.4 Conclusions 327 Acknowledgments 327 References 327 12.11.1 Introduction squalene. In a telling memoir, Teruo Ono recalls a statement by Konrad Bloch; the latter received the Nobel Prize for his The field of lipidomics unifies investigations of the great diver- studies of sterol biosynthesis, including discovery of the role of sity of lipids, including their cellular profiles, genes for their molecular oxygen in the reaction (Tchen and Bloch, 1957). biosynthetic pathways, and the enzymes these genes encode. Professor Bloch is reported to have said as early as 1976, “... Lipidomics is a word that appears frequently in the biomedical one can argue that any advantageous O2-dependent or O2uti- literature, where it is associated with metabolite profiling in lizing reactions – and sterol biosynthesis is one of these – must the characterization and treatment of disease (e.g., Wenk, [have involved an] aerobic prokaryotic partner. For this reason 2005). In parallel, geochemists have applied many of the the capacity of the methanotrophic bacteria to synthesize ste- same approaches to investigate the occurrence of lipid biosyn- rols assumes special significance” (Ono, 2002). The geologic thetic genes and enzymes in organisms that have relevance to and evolutionary implications of an O2-dependent lipid bio- ecosystem function, Earth history, and paleoclimatology. synthetic pathway were apparent to Professor Bloch, but it took Some of the earliest history of an integrated approach to several decades to determine that sterol biosynthesis has a lipidomics can be credited to studies of the cyclization of common history and requirement for O2 in both prokaryotes Treatise on Geochemistry 2nd Edition http://dx.doi.org/10.1016/B978-0-08-095975-7.01022-6 291 Treatise on Geochemistry, Second Edition, (2014), vol. 12, pp. 291-336 Author's personal copy 292 Lipidomics for Geochemistry and eukaryotes. Decoding the enzymatic underpinning of the 3 and 4 that are difficult to address. Molecular genetics experi- initial oxidative step required cloning the genes and expressing ments (e.g., Welander et al., 2010) and metagenomic approaches the epoxidase enzymes from yeast (Jandrositz et al., 1991) and (e.g., Pearson and Rusch, 2009) promise to aid these efforts, rat (Sakakibara et al., 1995), as well as solving the structure of as does a more frequent application of concomitant isotopic the sterol cyclase from humans (Thoma et al., 2004). Nearly in measurements – both at natural levels and in tracer experiments parallel, the squalene–hopene cyclases of Alicyclobacillus acid- (e.g., Waldbauer et al., 2011). ocaldarius (Ochs et al., 1990; Wendt et al., 1997) and Methylo- This chapter is not meant to be a comprehensive review of coccus capsulatus (Tippelt et al., 1998) also were characterized all lipidomic approaches. Rather, it is intended to serve as an and were confirmed to cyclize squalene to hopanoids in the introductory text. It describes the enzymes involved in some of absence of external oxidants. Based on comparative analysis of the major lipid biosynthetic pathways, it provides a framework these results, the mysterious presence of both hopanoids and for lipidomics-based approaches to geochemical questions, steroids in M. capsulatus (Bird et al., 1971) now is understood and it reviews several recent examples of case studies that use as resulting from the presence of genes for both the oxidative these approaches. The biosynthesis section provides the essen- (steroid) and direct cyclization (hopanoid) pathways in the tial underpinning for understanding relationships between genome of this organism (Lamb et al., 2007; Rohmer et al., enzymatic pathways and taxonomic groups. The applications 1980b), negating the alternative suggestion that a single path- section gives examples of lipidomics in practice, showing the way might perform both functions in the bacterium (Tippelt potential of these approaches to achieve a better understanding et al., 1998). Together, this framework illustrates how a of the origins of hydrocarbon ‘biomarker’ signatures preserved geologically relevant biochemistry – namely, a requirement in the geologic record. for O2 that is preserved in a recalcitrant biomarker – is under- stood via chemical and molecular methods. Such approaches are experiencing a rapid increase in popu- 12.11.2 Lipid Biosynthetic Pathways larity in association with the DNA sequencing revolution. In > particular, the observation that 99% of known microbial The two major families of lipids are called acetogenic and iso- diversity remains uncultured (Hugenholtz and Pace, 1996)has prenoid in reference to their respective monomeric units, acetate accelerated the application of lipidomic approaches to geoche- and isoprene. Isoprenoids are subdivided further into those mical problems, especially in the realm of geomicrobiology. that are synthesized via the mevalonic acid (MVA) pathway What lipids do these unstudied organisms make? How do we (Bloch et al., 1959; Lynen et al., 1958) and those that are link lipids and unknown taxa with contemporary environmental synthesized via the methylerythritol phosphate (MEP) pathway conditions and with the geologic record, given the vastness of (Rohmer et al., 1993). All cellular lipids contain core hydrocar- microbial diversity? These questions can be explored using the bon structures that are homogeneous polymers of one of these explosion of publicly available genomic data. To date, there are precursors. (N.b.: In this context, the important tetrapyrrole >2000 sequenced microbial species (http://www.ncbi.nlm.nih. classes of environmental biomarkers (e.g., porphyrins) are not gov/); 350 environmental metagenomes (the largest of which lipids, as their pyrrole units derive from amino acid precursors: remains the Global Ocean Sequencing project; Rusch et al., they are effectively modified protein. However, many of the 2007), including multiple examples using high-throughput principles discussed here could be applied equally to them.) sequencing methodologies (e.g., Dinsdale et al., 2008); and a few applications using single-cell genomics (e.g., Grindberg 12.11.2.1 Acetogenic Lipids et al., 2011). The biosynthetic potential encoded by this wealth of DNA data can provide tremendous insight into the phylo- Complex lipids containing a polar (often glyco- or phospho-) genetic distribution of lipid biosynthetic pathways. head group, glycerol backbone, and two esterified n-alkyl tails Geochemical studies that use lipidomics generally have one are the primary components of nearly all cell membranes. or more of the following objectives: Important exceptions occur in some bacteria, which substitute ether linkages for the ester bonds, yielding glycerol mono- and 1. Determine if a specific biosynthetic step or pathway is diethers (Caillon et al., 1983; DeRosa et al., 1988; Huber et al., present in a given organism. 1992; Langworthy et al., 1983) and/or diglycerol tetraethers 2.
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