Some of the marine environments, including hot vents, polar icy waters, acidic and alkaline waters, salt brines and pressurized abyssal trenches, present conditions so hostile to humans that they were initially considered too extreme to support microbial life. However, as sampling and laboratorial culture conditions techniques evolved, it was found that microbial “extremophiles” could survive and thrive in such environments [23]. They were named according to their optimal growth conditions as thermophiles (T_opt > 60 °C), hyperthermophiles (T_opt > 80 °C), psychrophiles (T_opt < 15 °C), acidophiles (pH_opt < 3), alkaliphiles (pH_opt > 8.5), halophiles (NaCl > 3%) and barophiles, or piezophiles. A few bacterial strains can endure both elevated temperature and extreme pH, being considered poly-extremophiles [24].

Extremophiles can be (i) obligate extremophiles, which only grow under one or more extreme conditions, and (ii) facultative extremophiles, which grow optimally at a non-extreme condition but can tolerate and thrive under conditions that are lethal or toxic to the majority of living organisms. Extremophiles present alterations in fatty acid composition of the cellular membranes and produce specialized lipids, allowing them to survive under conditions that kill most of the other micro-organisms.

Most of the marine environment is characterized by a temperature below 4 °C and pressure above 100 × 10⁵ Pa, favoring psychrophilic and barophilic bacteria [25]. During a one-year study with monthly sampling throughout the water column (from surface to 4750 m deep) in Hawaii, it was found that pelagic crenarchaeota, a group of archaea, was equivalent in cell numbers to bacteria at depths greater than 1000 m [2]. The authors estimated that the global oceans harbor approximately 1.3 × 10²⁸ archaeal cells and 3.1 × 10²⁸ bacterial cells. Biogeochemical and stable carbon isotopic analyses of a sedimentary record of archaeal lipids indicate that an anoxic event in Earth history led certain hyperthermophilic Archaea to adapt to low-temperature environments and to their massive expansion [26]. In subsurface sediments, buried deeper than 1 m in a wide range of oceanographic settings, it was found that at least 87% of intact polar membrane lipids could be attributable to archaeal membranes [27].

The fatty acid composition of the membrane phospholipids regulates membrane fluidity. At extremely low temperatures, an increase in the content of unsaturated and polyunsaturated fatty acids and a decrease in the average chain length of fatty acids in cellular membranes is observed [28,29]. Several psychrophilic bacterial strains isolated from sea ice produce a novel enzyme family required for the biosynthesis of PUFAs at low temperatures called polyketide synthase (PKS) [30,31]. The genes encoding these enzymes responsible for de novo long-chain PUFA biosynthesis are designated pfaEABCD and were thought to exist in the narrow subset of marine bacteria able to produce long-chain fatty acids [32]. However, the genetic potential to produce long-chain fatty acids via a FAS/PKS mechanism seems to be scattered throughout the bacterial domain [32]. During a stepwise adaptation of Rhodococcus erythropolis DCL14 cells from optimal growth conditions (28 °C, pH 7.0) to extreme conditions (that previously killed non-adapted cells) [13], it was found that the cells produced increased amounts of polyunsaturated fatty acids at lower temperatures and in the presence of copper sulphate (Figure 1). The cells produced 2.4 and 3.6 times more PUFAs at 15 and 4 °C, respectively, than at 28 °C (Figure 1A). A dose-dependent increase in the content of PUFAs was observed with copper sulphate for concentrations higher than 0.03% (w/v), reaching a 3.7-fold increase at 1% (Figure 1D). The pH and salt concentration did not significantly affected PUFA production in R. erythropolis (Figure 1B,C). A type Q gene cluster homologous to the pfa genes had been found in R. erythropolis PR4 [32].

Lipids are known to be heat-sensitive, and hyperthermophile bacteria produce special lipids. The bacterium Thermotoga maritima, which presents one of the highest growth temperatures at 90 °C, contains a novel glycerol ether lipid called 15,16-dimethyl-30-glyceryloxy-triacontanedioic acid that confers protection against hydrolysis at high temperatures [33]. The lipids of thermophilic archaea are characterized by unique structural features: they contain isoprenoid (phytanyl) chains with 15, 20, 25 or 40 carbons instead of straight chains observed in other organisms; two of these chains are linked via ether linkages to glycerol or a polyol; the glycerol found in archaea, 2,3-di-O-sn-glycerol, has the reverse stereochemistry when compared to that found in other organisms [34]. The ether lipids derived from diphytanyl-glycerol, or from its dimer di(biphytanyl)-diglycerol, are present on all archaeal membranes and confer to the cells a remarkable resistance against hydrolysis at high temperatures and acidic pH [35]. Furthermore, at high temperatures, an increased degree of cyclization of the aliphatic core of archaeal membranes is observed with a larger ratio of tetraether lipids vs. diether lipids, and the number of cyclopentane rings can vary up to four per aliphatic chain, thus maintaining membrane fluidity [36,37].

At high temperatures, thermophiles have problems keeping the intracellular concentration of Na⁺, since at a high temperature, the cell membrane becomes more permeable to the diffusion of protons and sodium ions [38]. Higher salinity concentrations cause, in general, an increase in the content of negatively charged phospholipids at the expense of neutral phospholipids. Gram-negative bacteria decrease the proportion of zwitterionic phosphatidylethanolamine in the membrane, while increasing the proportion of negatively charged phosphatidylglycerol and/or diphosphatidylglycerol [39,40]. In gram-positive bacteria, the anionic lipid fraction increases with salinity as a result of a higher content of diphosphatidylglycerol rather than phosphatidylglycerol [40].

When the transcriptional profiling of the halophile Halobacterium sp. NRC-1, which was among the first Archaea to be completely sequenced, was studied, it was found that growth at cold temperatures altered the expression of genes involved in lipid metabolism [41]. The gene coding for sn-1-glycerol phosphate dehydrogenase, responsible for the first step in the synthesis of polar lipids, was down regulated by 2.7-fold, while up-regulation was observed in the genes encoding for dehydrogenases for increased turnover of polar lipids, for a long-chain fatty acid-CoA ligase and for acetoacetyl-CoA thiolase, allowing the strain to alter the composition in lipids in the cold.

The fluidizing properties of EPA/DHA on cellular membranes seem a key point in barophilic bacteria, which have to carry out respiration at temperatures near 0 °C and under extremely high hydrostatic pressure. In Acholeoplasma laidlawii, when only 50% of the total lipids are in the fluid state, bacteria can still slowly grow and replicate, but growth ceases when around 90% of the membrane lipids pass from the liquid crystalline to the gel phase [42]. Although DHA and EPA phospholipids have an important role in disrupting or blocking the formation of islands of gel-phase lipids, there could be more fluidizing processes or lipids involved [15].

Two barophilic bacteria isolated from sediments from the Marianas Trench, DB21MT-2 and DB21MT-5, presented novel phospholipids in the classes of phosphatidylglycerol (PG) and phosphatidylethanolamine (PE) and its derivatives, phosphatidylmethylethanolamine (PME) and phosphatidyldimethylethanolamine (PDME) [43]. The phospholipids contained a high amount of 20:5ω3 (EPA; in DB21MT-2) and 22:6ω3 (DHA; in both strains) on the sn-1 and mostly on the sn-2 position of the phospholipids. Furthermore, the PUFAs were associated with almost every PG molecule, which was expected to cause greater disruption in acyl chain packing due to the larger head group of this phospholipid. The studies by Fang et al. [43] also suggested that psychrophilic and barophilic bacteria should be the major contributors of PUFAs to deep-sea sediments, since the vertical flux of PUFAs from surface water plankton decrease rapidly with depth.

The marine environment has favored the production of unique fatty acids and lipid molecules (Table 1). Bacterial fatty acids that can be used as biomarkers in marine environment are typically odd-numbered, branched trans-unsaturated and cyclopropyl fatty acids, e.g., 15:0, 17:0, 10-methyl-16:0, iso- and anteiso-branched saturated and monounsaturated [5]. Besides phospholipids, fatty acids are the building blocks of other lipid classes, including ceramides, wax esters, glycosphingolipids and N-acylated lipid molecules. Cyanobacteria are a source of acylated lipids and fatty acid amides [5]. The marine cyanobacterium Oscillatoria sp. produces a new diacylgalactolipid comprising 9,12-octadecadienoyl and 4-hexadecenoyl chains [44], whilst Lyngbya majuscule produces bioactive secondary malyngamides, such as Malyngamide G and 7-methoxydodec-4(E)-enoic acid [45,46].

Extremophiles are also good sources of unusual fatty acids. Psychrophilic Bacillus species produce relatively rare Δ⁵-isomers, although no obvious advantage for growth at low temperature is provided by these isomers when compared to membrane lipids with Δ⁹- or Δ¹¹-isomers [47]. Bacteroides fragilis produces a branched-chain hydroxyl fatty acid in the amide for 3-hydroxy-15-methylhexadecanoic acid in lipopolysaccharides, which is rather specific in gram-negative bacteria [48]. The archaea Thermoplasma acidophilum, whose optimal growth conditions are 55–59 °C and pH 1–2, produces a peculiar membrane with 82% polar lipids having as the main polar lipid a bipolar tetraether lipid with a phosphoglycerol and a β-L-gulopyranose as head groups and up to four cyclopentane rings per aliphatic chain [37].

In a recently published paper, Sanchez et al. [49] examined for the first time a fish microbiome to isolate bacteria able to produce unique marine natural products. The fish intestines were a source of Actinomycetales, as well as unique strains of Firmicutes and Proteobacteria. The chemical extracts contained a new bioactive lipid called sebastenoic acid, which has anti-microbial activity against Staphylococcus aureus, Bacillus subtilis, Enterococcus faecium and Vibrio mimicus.

Furan fatty acids, shown to be scavengers of hydroxyl and peroxyl radicals and to provide potential protective properties in mammalian tissue and blood, have been found in, e.g., marine sponges, algae, plants and also in marine bacteria, such as Shewanella putrefaciens [50,51]. These acids are tri- or tetra-substituted furan derivatives characterized by either a propyl or pentyl side chain in one of the α-positions and a substituted straight long-chain saturated acid with a carboxylic group at its end on the other.

The analyses of phospholipid-based fatty acids (PLFAs) were introduced as a means to assess live bacterial biomass, since they are rapidly degraded after cell death [21]. However a surface sediment from Carteau cove, France, contained, apart from phospholipids, non-phospholipid polar compounds with 12- to 28-carbon atoms, which cautions against the use of PLFAs to assess bacterial biomass without preliminary analysis and purification of phospholipids [54].

Some bacteria incorporate fatty acids containing furan in their phospholipids. Among the species able to produce furan acids are Shewanella putrefaciens, Marinomonas comunis, Enterobacter agglomerans and Pseudomonas fluorescens, which were isolated from the intestinal liquor of fishes [55]. It was proposed that in marine bacteria living in fish, furan acids are generated by incorporation of a methyl group into cis-vaccenic acid, followed by introduction of a second double bond, and the diunsaturated fatty acid formed is presumed to react with oxygen, followed by ring closure, to assume the final furan acid structure [51]. These acids present a radical-scavenging ability and should help in protecting the cells [50].

Marine oil-degrading or hydrocarbonoclastic bacteria usually produce significant amounts of neutral lipids, which can be used as storage compounds, probably as a result of sporadic availability of hydrocarbons as growth substrates [56,57]. Among these compounds are triacylglycerols, diacylglycerols, wax esters and polyhydroxyalkanoates. The marine hydrocarbonoclastic bacterium Marinobacter sp. PAD-2 produced extracellular wax ester-like compounds when grown on hexadecane or succinate as the sole carbon source [57]. When Alvarez et al. tested forty psychrophile or psychrotrophic crude oil-utilizing bacteria, they found that around 73% of the strains were able to accumulate specialized lipids, such as polyhydroalkanoic acids (PHAs), and two strains were able to produce wax esters as storage compounds [56]. PHA accumulation was predominantly observed between 4 and 20 °C.

A R. erythropolis strain, able to degrade hydrocarbons and fuel oil under saline conditions [58], produces and excretes a trehalose based glycolipid to increase the bioavailability of hydrocarbons with reduced water solubility, and also when the cells are dehydrated (Figure 2). Extracellular polymeric substances provide protection for microbial cells, resulting in increased resilience under stressful periods [59]. Among the best examples of temporary stresses are marine intertidal conditions. In this case, micro-organisms are mainly in immobilized communities called biofilms, which confer protection against high temperature and exposure to ultraviolet radiation, temporary dehydration, limited access to nutrients and competition [60]. Curiously, intertidal bacteria have also been found to be a good source of PUFAs, with Shewanella colwelliana, Vibrio splendidus and Photobacterium lipolyticum being isolated from anoxic intertidal sediments [61].

The potentials for fatty acid and PUFA synthesis in HP are closely related to phylogenetic lineages (see Desvilettes & Bec and references therein [95]). Nevertheless, previous studies have identified two main factors affecting the PUFA composition of HP related to their habitat (marine vs. freshwater) and diet origin (bacteria vs. algae). While in freshwater HP ω6 FA dominate PUFA, marine HP contain high levels of ω3 highly unsaturated FA (HUFA), like EPA and DHA [100,101]. Both marine and freshwater HP feeding on algae have a higher content of ω3 PUFA than when feeding on bacteria [102,103], probably resulting from the higher availability of ω3 PUFA in algae. Most protists synthesize PUFA through a series of aerobic desaturations and elongations of the 16:0 and 18:0 acids produced by fatty acid synthase (FAS). Marine protists, namely thraustochytrids, are also able to produce PUFA using the PKS pathway and accumulate them in triacylglycerols [104,105]. Thraustochytrids, which are abundant in the marine foodweb, may be an important source of PUFA for the higher trophic levels [106]. In fact, thraustochytrids that may feed on bacteria are considered an alternative to fish oils as a source of long-chain PUFA [102] and are established candidates for commercial production of DHA [107].

Bacteria usually do not produce sterols, although there is evidence that some eubacteria are capable of synthesizing sterols de novo (e.g., Methylococcus capsulatus [108]). Crustaceans usually obtain their sterols directly via algae or through HP that have been feeding on algae. Some heterotrophic flagellates have the ability to synthesize sterols de novo [98], although ciliates seem to lack this ability. In the absence of dietary sterols, as when feeding on bacteria, ciliates produce the pentacyclic triterpenoid alcohol tetrahymanol or hopanoids, which serve as sterol surrogates in cell membranes (see Martin-Creuzburg and von Elert, and reference therein [109]). Some crustaceans (e.g., copepods) may incorporate tetrahymanol into their tissues, which enables them to maintain minimal egg production. Nevertheless, as Martin-Creuzburg and von Elert noted, it hasn’t been tested whether tetrahymanol or hopanoids improve the performance of crustaceans. Nevertheless, the production of sterols or functionally equivalent compounds, like tetrahymanol, by intermediary protozoans may improve carbon transfer efficiency via the microbial loop from nutritionally inadequate primary producers to metazoan grazers.