Hopanoids

Hopanoids are a diverse subclass of triterpenoids with the same hydrocarbon skeleton as the compound hopane. This group of pentacyclic molecules therefore refers to simple hopenes, hopanols and hopanes, but also to extensively functionalized derivatives such as bacteriohopanepolyols (BHPs) and hopanoids covalently attached to lipid A.[1][2]

Some representative hopanoids: A. Diploptene, also called 22(29)-hopene B. Diplopterol, also called hopan-22-ol, the hydrated cyclomer of diploptene C. Bacteriohopanetetrol (BHT), a common extended hopanoid D. Hopane, the diagenetic product of A and B that results from reducing conditions during deposition and persists in the rock record. The diagenetic product of C would be an extended C35 hopane.
Cholesterol, a sterol compound found in all eukaryotes.

The first known hopanoid, hydroxyhopanone, was isolated by two chemists at The National Gallery, London working on the chemistry of dammar gum, a natural resin used as a varnish for paintings.[3] While hopanoids are often assumed to be made only in bacteria, their name actually comes from the abundance of hopanoid compounds in the resin of plants from the genus Hopea. In turn, this genus is named after John Hope, the first Regius Keeper of the Royal Botanic Garden, Edinburgh.

Since their initial discovery in an angiosperm, hopanoids have been found in plasma membranes of bacteria, lichens, bryophytes, ferns, tropical trees and fungi.[4] Hopanoids have stable polycyclic structures that are well-preserved in petroleum reservoirs, rocks and sediment, allowing the diagenetic products of these molecules to be interpreted as biomarkers for the presence of specific microbes and potentially for chemical or physical conditions at the time of deposition.[5] Hopanoids have not been detected in archaea.[6][7]

Biological function

About 10% of sequenced bacterial genomes have a putative shc gene encoding a squalene-hopene cyclase and can presumably make hopanoids, which have been shown to play diverse roles in the plasma membrane and may allow some organisms to adapt in extreme environments.[8][9]

Since hopanoids modify plasma membrane properties in bacteria, they are frequently compared to sterols (e.g., cholesterol), which modulate membrane fluidity and serve other functions in eukaryotes.[10] Although hopanoids do not rescue sterol deficiency, they are thought to increase membrane rigidity and decrease permeability.[9][11][12] Also, gammaproteobacteria and eukaryotic organisms such as lichens and bryophytes have been shown to produce both sterols and hopanoids, suggesting these lipids may have other distinct functions.[4][13] Notably, the way hopanoids pack into the plasma membrane can change depending on what functional groups are attached. The hopanoid bacteriohopanetetrol assumes a transverse orientation in lipid bilayers, but diploptene localizes between the inner and outer leaflet, presumably thickening the membrane to decrease permeability.[14]

The hopanoid diplopterol orders membranes by interacting with lipid A, a common membrane lipid in bacteria, in ways similar to how cholesterol and sphingolipids interact in eukaryotic plasma membranes.[10] Diplopterol and cholesterol were demonstrated to promote condensation and inhibit gel-phase formation in both sphingomyelin monolayers and monolayers of glycan-modified lipid A. Furthermore, both diplopterol and cholesterol could rescue pH-dependent phase transitions in glycan-modified lipid A monolayers.[10] The role of hopanoids in membrane-mediated acid tolerance is further supported by observations of acid-inhibited growth and morphological abnormalities of the plasma membrane in hopanoid-deficient bacteria with mutant squalene-hopene cyclases.[15][16]

Hopanoids are produced in several nitrogen-fixing bacteria.[9] In the actinomycete Frankia, hopanoids in the membranes of vesicles specialized for nitrogen fixation likely restrict the entry of oxygen by making the lipid bilayer more tight and compact.[17] In Bradyrhizobium, hopanoids chemically bonded to lipid A increase membrane stability and rigidity, enhancing stress tolerance and intracellular survival in Aeschynomene legumes.[18] In the cyanobacterium Nostoc punctiforme, large quantities of 2-methylhopanoids localize to the outer membranes of survival structures called akinetes.[19] In another example of stress tolerance, hopanoids in the aerial hyphae (spore bearing structures) of the prokaryotic soil bacteria Streptomyces are thought to minimize water loss across the membrane to the air.[20]

Biosynthesis

Squalene synthesis

Since hopanoids are a C₃₀ terpenoid, biosynthesis begins with isopentenyl pyrophosphate (IPP) and dimethylallyl pyrophosphate (DMAP), which are combined to form longer chain isoprenoids.[2] Synthesis of these smaller precursors proceeds either via the mevalonate pathway or the methylerythritol-4-phosphate pathway depending on the bacterial species, although the latter tends to be more common.[21] DMAP condenses with one molecule of IPP to geranyl pyrophosphate, which in turn condenses with another IPP to generate farnesyl pyrophosphate (FPP).[2] Squalene synthase, coded for by the gene sqs, then catalyzes the condensation of two FPP molecules to presqualene pyrophosphate (PSPP) before oxidizing NADPH to release squalene.[22] However, some hopanoid-producing bacteria lack squalene synthase and instead use the three enzymes HpnC, HpnD and HpnE, which are encoded in the hpn operon with many other hopanoid biosynthesis genes.[23] In this alternative yet seemingly more widespread squalene synthesis pathway, HpnD releases pyrophosphate as it condenses two molecules of FPP to PSPP, which HpnC converts to hydroxysqualene, consuming a water molecule and releasing another pyrophosphate. Then, hydroxysqualene is reduced to squalene in a dehydration reaction mediated by the FAD-dependent enzyme HpnE.[22]

Active site of the squalene-hopene cyclase from Methylococcus capsulatus engaging the substrate, squalene, shown in gold. The cyclase is depicted as a monomer.

Cyclization
Alpha barrel structure of the squalene-hopene cyclase from Methylococcus capsulatus. Alpha helices are shown in blue, loop regions in green, and beta sheets in red.

Next, a squalene-hopene cyclase catalyzes an elaborate cyclization reaction, engaging squalene in an energetically favorable all-chair conformation before creating 5 cycles, 6 covalent bonds, and 9 chiral centers on the molecule in a single step.[24][25] This enzyme, coded for by the gene shc (also called hpnF in some bacteria), has a double ⍺-barrel fold characteristic of terpenoid biosynthesis[26] and is present in the cell as a monotopic homodimer, meaning pairs of the cyclase are embedded in but do not span the plasma membrane.[24][27] In vitro, this enzyme exhibits promiscuous substrate specificity, also cyclizing 2,3-oxidosqualene.[28]

Aromatic residues in the active site form several unfavorable carbocations on the substrate which are quenched by a rapid polycyclization.[25] In the last substep of the cyclization reaction, after electrons comprising the terminal alkene bond on the squalene have attacked the hopenyl carbocation to close the E ring, the C-22 carbocation may be quenched by mechanisms that lead to different hopanoid products. Nucleophilic attack of water will yield diplopterol, while deprotonation at an adjacent carbon will form one of several hopene isomers, often diploptene.[4]

Functionalization

After cyclization, hopanoids are frequently modified by hopanoid biosynthesis enzymes encoded by genes in the same operon as shc, hpn.[29] For instance, the radical SAM protein HpnH adds an adenosine group to diploptene, forming the extended C35 hopanoid adenosylhopane, which can then be further functionalized by other hpn gene products.[30] HpnG catalyzes the removal of adenine from adenosylhopane to make ribosyl hopane, which reacts to form bacteriohopanetetrol (BHT) in a reaction mediated by an unknown enzyme.[31] Additional modifications may occurs as HpnO aminates the terminal hydroxyl on BHT, producing amino bacteriohopanetriol, or as the glycosyltransferase HpnI converts BHT to N-acetylglucosaminyl-BHT.[32] In sequence, the hopanoid biosynthesis associated protein HpnK mediates deacetylation to glucosaminyl-BHT, from which radical SAM protein HpnJ generates a cyclitol ether.[32]

Importantly, C30 and C35 hopanoids alike may be methylated at C-2 and C-3 positions by the radical SAM methyltransferases HpnP and HpnR, respectively.[33][34] These two methylations are particularly geostable compared to side-chain modifications and have entertained geobiologists for decades.[9]

In a biosynthetic pathway exclusive to some bacteria, the enzyme tetrahymanol synthase catalyzes the conversion of the hopanoid diploptene to the pentacyclic triterpenoid tetrahymanol. In eukaryotes like Tetrahymena, tetrahymanol is instead synthesized directly from squalene by a cyclase with no homology to the bacterial tetrahymanol synthase.[35]

In paleobiology

Hopanoids have been estimated to be the most abundant natural products on Earth, remaining in the organic fraction of all sediments, independent of age, origin or nature.[36] Biomolecules like DNA and proteins are degraded during diagenesis, but polycyclic lipids persist in the environment over geologic timescales due to their fused, stable structures.[37] Although hopanoids and sterols are reduced to hopanes and steranes during deposition, these diagenetic products can still be useful biomarkers, or molecular fossils, for studying the coevolution of early life and Earth.[37][38]

2-methylhopanes supposedly from photosynthetic cyanobacteria and steranes were reported by Roger Summons and colleagues as molecular fossils preserved in 2.7 Gya shales from the Pilbara region in Western Australia.[39] The presence of abundant 2-alpha-methylhopanes preserved in these shales was interpreted as evidence of oxygenic photosynthesis at least 2.7 Gya, unexpectedly suggesting a 400 million year gap between the evolution of oxygenic metabolism and when Earth’s atmosphere became oxidizing. This interpretation of the biomarker record was challenged when Geobacter sulfurreducens was demonstrated to synthesize diverse hopanols, although not 2-methyl-hopanols, when grown under strictly anaerobic conditions.[8] The integrity of 2-methylhopanes as biomarkers for oxygenic photosynthesis was then further attenuated by evidence that the phototroph Rhodopseudomonas palustris produced 2-methyl-BHPs only under anoxic conditions.[40] Concrete evidence came from studies showing that not all cyanobacteria make hopanoids and that genes coding for the methyltransferase HpnP are present in nonphotosynthetic alphaproteobacteria and acidobacteria.[33][41]

Biomarker findings in the Pilbara-Craton shales were later rejected altogether during more recent evaluations of the fossil triterpenoid record.[42] Currently, the oldest detected triterpenoid fossils are Mesoproterozoic okenanes, steranes, and methylhopanes from a 1.64 Gya basin in Australia.[43] However, molecular clock analyses estimate that the earliest sterols were likely produced around 2.3 Gya, around the same time as the Great Oxidation Event, with hopanoid synthesis arising even earlier.[44]

For several reasons, hopanoids and squalene-hopene cyclases have been hypothesized to be more ancient than sterols and oxidosqualene cyclases. First, diplopterol is synthesized when water quenches the C-22 carbocation formed during polycyclization. This indicates that hopanoids can be made without molecular oxygen and could have served as a sterol surrogate before the atmosphere accumulated oxygen, which reacts with squalene in a reaction catalyzed by squalene monooxygenase during sterol biosynthesis.[1] Furthermore, squalene binds to squalene-hopene cyclases in a low-energy, all-chair conformation while oxidosqualene is cyclized in a more strained, chair-boat-chair-boat conformation.[4][45] Squalene-hopene cyclases also display more substrate promiscuity in that they cyclize oxidosqualene in vitro, causing some scientists to hypothesize that they are evolutionary predecessors to oxidosqualene cyclases.[45] Other scientists have proposed that squalene-hopene and oxidosqualene cyclases diverged from a common ancestor, a putative bacterial cyclase that would have made a tricyclic malabaricanoid or tetracyclic dammaranoid product.[1][46]

Industrial Relevance

The elegant mechanism behind the protonase activity of squalene-hopene cyclase was appreciated and adapted by chemical engineers at the University of Stuttgart, Germany. Active site engineering resulted in loss of the enzyme's ability to form hopanoids, but enabled Brønsted acid catalysis for the stereoselective cyclization of the monoterpenoids geraniol, epoxygeraniol, and citronellal.[47]

Agricultural Relevance

The application of hopanoids and hopanoid-producing nitrogen fixers to soil has been proposed and patented as a biofertilizer technique that increases environmental resistance of plant-associated microbial symbionts, including nitrogen-fixing bacteria that are essential for transforming atmospheric nitrogen to soluble forms available to crops.[48]

Medical Relevance

During later studies of interactions between diplopterol and lipid A in Methylobacterium extorquens, multidrug transport was found to be a hopanoid-dependent process. Squalene-hopene cyclase mutants derived from a wild type capable of multidrug efflux, a drug-resistance mechanism mediated by integral transport proteins, lost the ability to perform both multidrug transport and hopanoid synthesis.[12] Researchers indicate this could be due to direct regulation of transport proteins by hopanoids or indirectly by altering membrane ordering in a way that disrupts the transport system.[12]

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