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Kharbush, JJ, Allen AE, Moustafa A, Dorrestein PC, Aluwihare LI.  2016.  Intact polar diacylglycerol biomarker lipids isolated from suspended particulate organic matter accumulating in an ultraoligotrophic water column. Organic Geochemistry. 100:29-41.   10.1016/j.orggeochem.2016.07.008   Abstract

Intact polar diacylglycerols (IP-DAGs) are essential components of cell membranes. Because they are structurally diverse and hypothesized to represent primarily living cells, they are potential molecular markers for a recent contribution by microbial communities to various carbon reservoirs. This study employed a novel molecular networking approach to investigate the evolution of IP-DAG structural diversity with depth in an ultraoligotrophic environment of the western South Pacific Ocean to test the hypothesis that particle transport to depth is rapid enough to preserve the IP-DAG biomarker signature of the photosynthetic community. IP-DAG profiles of several cultured cyanobacteria and photosynthetic picoeukaryotes were used as templates for constructing molecular networks to compare and interpret IP-DAG signatures of suspended particles isolated from a water column depth profile. Analysis of corresponding genetic community composition data for the same field samples was used to connect IP-DAG structures with their likely biological sources. Our data show that, although most IP-DAG classes associated with photosynthetic organisms were not observed below the euphotic zone, several other IP-DAG classes in deep samples might provide interesting targets for future studies seeking to examine the in situ contribution of deep sea microbes to suspended particulate organic matter (POM). Overall, the results represent the deepest water column IP-DAG dataset to date and demonstrate the utility of molecular networking for analyzing and visualizing complex environmental datasets.

Kharbush, JJ, Ugalde JA, Hogle SL, Allen EE, Aluwihare LI.  2013.  Composite bacterial hopanoids and their microbial producers across oxygen gradients in the water column of the California Current. Applied and Environmental Microbiology.   10.1128/aem.02367-13   AbstractWebsite

Hopanoids are pentacyclic triterpenoid lipids produced by many prokaryotes as cell membrane components. The structural variations of composite hopanoids, or bacteriohopanepolyols (BHPs), produced by various bacterial genera makes them potentially useful molecular biomarkers of bacterial communities and metabolic processes, in both modern and ancient environments. Building on previous work suggesting that organisms in low-oxygen environments are important contributors to BHP production in the marine water column and that there may be physiological roles for BHPs specific to these environments, this study investigated the relationship between trends in BHP structural diversity and abundance and the genetic diversity of BHP producers for the first time in a low-oxygen environment of the Eastern Tropical North Pacific. Amplification of the hopanoid biosynthesis gene, squalene hopene cyclase (sqhC), indicated far greater genetic diversity than would be predicted by examining BHP structural diversity alone, and that greater sqhC genetic diversity exists in the marine environment than is represented by cultured representatives and most marine metagenomes. In addition, the genetic relationships in this dataset suggest microaerophilic environments as potential “hot spots” of BHP production. Finally, structural analysis of BHPs showed that an isomer of the commonly-observed BHP bacteriohopanetetrol (BHT) may be linked to a producer that is more abundant in low-oxygen environments. Results of this study increase the known diversity of BHP producers and provide a detailed phylogeny with implications for the role of hopanoids in modern bacteria as well as the evolutionary history of hopanoid biosynthesis, both of which are important considerations for future interpretations of the marine sedimentary record.

Kharbush, JJ, Thompson LR, Haroon MF, Knight R, Aluwihare LI.  2018.  Hopanoid-producing bacteria in the Red Sea include the major marine nitrite oxidizers. Fems Microbiology Ecology. 94   10.1093/femsec/fiy063   AbstractWebsite

Hopanoids, including the extended side chain-containing bacteriohopanepolyols, are bacterial lipids found abundantly in the geological record and across Earth's surface environments. However, the physiological roles of this biomarker remain uncertain, limiting interpretation of their presence in current and past environments. Recent work investigating the diversity and distribution of hopanoid producers in the marine environment implicated low-oxygen regions as important loci of hopanoid production, and data from marine oxygen minimum zones suggested that the dominant hopanoid producers in these environments are nitrite-utilizing organisms, revealing a potential connection between hopanoid production and the marine nitrogen cycle. Here, we use metagenomic data from the Red Sea to investigate the ecology of hopanoid producers in an environmental setting that is biogeochemically distinct from those investigated previously. The distributions of hopanoid production and nitrite oxidation genes in the Red Sea are closely correlated, and the majority of hopanoid producers are taxonomically affiliated with the major marine nitrite oxidizers, Nitrospinae and Nitrospirae. These results suggest that the relationship between hopanoid production and nitrite oxidation is conserved across varying biogeochemical conditions in dark ocean microbial ecosystems.

Kharbush, JJ, Kejriwal K, Aluwihare LI.  2016.  Distribution and abundance of hopanoid producers in low-oxygen environments of the Eastern Pacific Ocean. Microbial Ecology. 71:401-408.   10.1007/s00248-015-0671-y   AbstractWebsite

Hopanoids are bacterial membrane lipid biomarker molecules that feature prominently in the molecular fossil record. In the modern marine water column, recent reports implicate bacteria inhabiting low-oxygen environments as important sources of hopanoids to marine sediments. However, the preliminary biogeography reported by recent studies and the environmental conditions governing such distributions can only be confirmed when the numerical abundance of these organisms is known with more certainty. In this study, we employ two different approaches to examine the quantitative significance of phylogenetically distinct hopanoid producers in low-oxygen environments. First, we develop a novel quantitative PCR (qPCR) assay for the squalene hopene cyclase (sqhC) gene, targeting a subset of hopanoid producers previously identified to be important in the eastern North Pacific Ocean. The results represent the first quantitative gene abundance data of any kind for hopanoid producers in the marine water column and show that these putative alphaproteobacterial hopanoid producers are rare, comprising at most 0.2 % of the total bacterial community in our samples. Second, a complementary analysis of existing low-oxygen metagenomic datasets further examined the generality of the qPCR observation. We find that the dominant sqhC sequences in these metagenomic datasets are associated with phyla such as Nitrospinae rather than Proteobacteria, consistent with the qPCR finding that alphaproteobacterial hopanoid producers are not very abundant in low-oxygen environments. In fact, positive correlations between sqhC gene abundance and environmental parameters in these samples identify nitrite availability as a potentially important factor in the ecology of hopanoid producers that dominate low-oxygen environments.

Kumar, A, Borgen M, Aluwihare LI, Fenical W.  2017.  Ozone-activated halogenation of mono- and dimethylbipyrrole in seawater. Environmental Science & Technology. 51:589-595.   10.1021/acs.est.6b03601   AbstractWebsite

Polyhalogenated N-methylbipyrroles of two different structure classes have been detected worldwide in over 100 environmental samples including seawater, bird eggs, fish, dolphin blubber, and in the breast milk of humans that consume seafood. These molecules are concentrated in the fatty tissues in comparable abundance to some of the most important anthropogenic contaminants, such as the halogenated flame-retardants and pesticides. Although the origin of these compounds is still unknown, we present evidence that the production of these materials can involve the direct ozone activated seawater halogenation of N-methylbipyrrole precursors. This observation shows that environmental polyhalogenated bipyrroles can be produced via an abiotic process, and implies that the ozone activated halogenation of a variety of natural and anthropogenic seawater organics may be a significant process occurring in surface ocean waters.