Steroids, triterpenoids and molecular oxygen

There is a close connection between modern-day biosynthesis of particular triterpenoid biomarkers and presence of molecular oxygen in the environment. Thus, the detection of steroid and triterpenoid hydrocarbons far back in Earth history has been used to infer the antiquity of oxygenic photosynthesis. This prompts the question: were these compounds produced similarly in the past? In this paper, we address this question with a review of the current state of knowledge surrounding the oxygen requirement for steroid biosynthesis and phylogenetic patterns in the distribution of steroid and triterpenoid biosynthetic pathways. The hopanoid and steroid biosynthetic pathways are very highly conserved within the bacterial and eukaryotic domains, respectively. Bacteriohopanepolyols are produced by a wide range of bacteria, and are methylated in significant abundance at the C2 position by oxygen-producing cyanobacteria. On the other hand, sterol biosynthesis is sparsely distributed in distantly related bacterial taxa and the pathways do not produce the wide range of products that characterize eukaryotes. In particular, evidence for sterol biosynthesis by cyanobacteria appears flawed. Our experiments show that cyanobacterial cultures are easily contaminated by sterol-producing rust fungi, which can be eliminated by treatment with cycloheximide affording sterol-free samples. Sterols are ubiquitous features of eukaryotic membranes, and it appears likely that the initial steps in sterol biosynthesis were present in their modern form in the last common ancestor of eukaryotes. Eleven molecules of O(2) are required by four enzymes to produce one molecule of cholesterol. Thermodynamic arguments, optimization of function and parsimony all indicate that an ancestral anaerobic pathway is highly unlikely. The known geological record of molecular fossils, especially steranes and triterpanes, is notable for the limited number of structural motifs that have been observed. With a few exceptions, the carbon skeletons are the same as those found in the lipids of extant organisms and no demonstrably extinct structures have been reported. Furthermore, their patterns of occurrence over billion year time-scales correlate strongly with environments of deposition. Accordingly, biomarkers are excellent indicators of environmental conditions even though the taxonomic affinities of all biomarkers cannot be precisely specified. Biomarkers are ultimately tied to biochemicals with very specific functional properties, and interpretations of the biomarker record will benefit from increased understanding of the biological roles of geologically durable molecules

Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II

Two major geological problems regarding the origin of oxygenic photosynthesis are (i) identifying a source of oxygen pre-dating the biological oxygen production and capable of driving the evolution of oxygen tolerance, and (ii) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically produced H2O2 at the surface of the glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H2O2, which interacts with seawater to produce O2 in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H2O2. Answers to the second problem are controversial and range from 3.8 to 2.2 Gyr ago. A sceptical view, based on the metals that have the redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the Late Archaean atmosphere (less than 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date 2.7 Gyr ago or above, and could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two

A comparative ToF-SIMS and GC–MS analysis of phototrophic communities collected from an alkaline silica-depositing hot spring

One of few techniques that is able to spatially resolve chemical data, including organic molecules, to morphologicalfeatures in modern and ancient geological samples, is time-of-flight secondary ion mass spectrometry(ToF-SIMS). The ability to connect chemical data to morphology is key for interpreting thebiogenicity of preserved remains in ancient samples. However, due to the lack of reference data for geologicallyrelevant samples and the ease with which samples can be contaminated, ToF-SIMS data may bedifficult to interpret. In this project, we aimed to build a ToF-SIMS spectral database by performing parallelToF-SIMS and gas chromatography–mass spectrometry (GC–MS) analyses of extant photosyntheticmicrobial communities collected from an alkaline silica-depositing hot spring in Yellowstone NationalPark, USA. We built the library by analyzing samples of increasing complexity: pure lipid standards commonlyfound in thermophilic phototrophs, solvent extracts of specific lipid fractions, total lipid extracts,pure cultures of dominant phototrophic community members, and unsilicified phototrophic streamercommunities.The results showed that important lipids and pigments originating from phototrophs were detected byToF-SIMS (e.g., wax esters, monogalactosyldiacylglycerol, digalactosyldiacylglycerol, sufloquinovosyldiaglycerol,alkanes, etc.) in the streamer lipid extracts. Many of the lipids were also detected in situin the unsilicified streamer, and could even be spatially resolved to individual cells within the streamercommunity. Together with the ToF-SIMS database, this mapping ability will be used to further exploreother microbial mats and their fossilized counterparts in the geological record. This is likely to expandthe geochemical understanding of these types of samples

Evolutionary innovation: a bone-eating marine symbiosis

Symbiotic associations between microbes and invertebrates have resulted in some of the most unusual physiological and morphological adaptations that have evolved in the animal world. We document a new symbiosis between marine polychaetes of the genus Osedax and members of the bacterial group Oceanospirillales, known for heterotrophic degradation of complex organic compounds. These organisms were discovered living on the carcass of a grey whale at 2891 m depth in Monterey Canyon, off the coast of California. The mouthless and gutless worms are unique in their morphological specializations used to obtain nutrition from decomposing mammalian bones. Adult worms possess elaborate posterior root-like extensions that invade whale bone and contain bacteriocytes that house intracellular symbionts. Stable isotopes and fatty acid analyses suggest that these unusual endosymbionts are likely responsible for the nutrition of this locally abundant and reproductively prolific deep-sea worm

Sources for sedimentary bacteriohopanepolyols as revealed by 16S rDNA stratigraphy

Bacteriohopanoids are widespread lipid biomarkers in the sedimentary record. Many aerobic and anaerobic bacteria are potential sources of these lipids which sometimes complicates the use of these biomarkers as proxies for ecological and environmental changes. Therefore, we applied preserved 16S ribosomal RNA genes to identify likely Holocene biological sources of bacteriohopanepolyols (BHPs) in the sulfidic sediments of the permanently stratified postglacial Ace Lake, Antarctica. A suite of intact BHPs were identified, which revealed a variety of structural forms whose composition differed through the sediment core reflecting changes in bacterial populations induced by large changes in lake salinity. Stable isotopic compositions of the hopanols formed from periodic acid-cleaved BHPs, showed that some were substantially depleted in 13C, indicative of their methanotrophic origin. Using sensitive molecular tools, we found that Type I and II methanotrophic bacteria (respectively Methylomonas and Methylocystis) were unique to the oldest lacustrine sediments (> 9400 years BP), but quantification of fossil DNA revealed that the Type I methanotrophs, including methanotrophs related to methanotrophic gill symbionts of deep-sea cold-seep mussels, were the main precursors of the 35-amino BHPs (i.e. aminopentol, -tetrol and -triols). After isolation of the lake ~3000 years ago, one Type I methanotroph of the 'methanotrophic gill symbionts cluster' remained the most obvious source of aminotetrol and -triol. We, furthermore, identified a Synechococcus phylotype related to pelagic freshwater strains in the oldest lacustrine sediments as a putative source of 2-methylbacteriohopanetetrol (2-Me BHT). This combined application of advanced geochemical and paleogenomical tools further refined our knowledge about Holocene biogeochemical processes in Ace Lake. © 2008 The Authors