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Impact of temperature on ladderane lipid distribution in anammox bacteria.

ABSTRACT: Anaerobic ammonium-oxidizing (anammox) bacteria have the unique ability to synthesize fatty acids containing linearly concatenated cyclobutane rings, termed "ladderane lipids." In this study we investigated the effect of temperature on the ladderane lipid composition and distribution in anammox enrichment cultures, marine particulate organic matter, and surface sediments. Under controlled laboratory conditions we observed an increase in the amount of C(20) [5]-ladderane fatty acids compared with the amount of C(18) [5]-ladderane fatty acids with increasing temperature and also an increase in the amount of C(18) [5]-ladderane fatty acids compared with the amount of C(20) [5]-ladderane fatty acids with decreasing temperature. Combining these data with results from the natural environment showed a significant (R(2) = 0.85, P = <0.0001, n = 121) positive sigmoidal relationship between the amounts of C(18) and C(20) [5]-ladderane fatty acids and the in situ temperature; i.e., there is an increase in the relative abundance of C(18) [5]-ladderane fatty acids at lower temperatures and vice versa, particularly at temperatures between 12 degrees C and 20 degrees C. Novel shorter (C(16)) and longer (C(22) to C(24)) ladderane fatty acids were also identified, but their relative amounts were small and did not change with temperature. The adaptation of ladderane fatty acid chain length to temperature changes is similar to the regulation of common fatty acid composition in other bacteria and may be the result of maintaining constant membrane fluidity under different temperature regimens (homeoviscous adaptation). Our results can potentially be used to discriminate between the origins of ladderane lipids in marine sediments, i.e., to determine if ladderanes are produced in situ in relatively cold surface sediments or if they are fossil remnants originating from the warmer upper water column.

SUBMITTER: Rattray JE

PROVIDER: S-EPMC2832374 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Impact of temperature on ladderane lipid distribution in anammox bacteria.

Rattray Jayne E JE van de Vossenberg Jack J Jaeschke Andrea A Hopmans Ellen C EC Wakeham Stuart G SG Lavik Gaute G Kuypers Marcel M M MM Strous Marc M Jetten Mike S M MS Schouten Stefan S Sinninghe Damsté Jaap S JS

Applied and environmental microbiology 20100104 5

Anaerobic ammonium-oxidizing (anammox) bacteria have the unique ability to synthesize fatty acids containing linearly concatenated cyclobutane rings, termed "ladderane lipids." In this study we investigated the effect of temperature on the ladderane lipid composition and distribution in anammox enrichment cultures, marine particulate organic matter, and surface sediments. Under controlled laboratory conditions we observed an increase in the amount of C(20) [5]-ladderane fatty acids compared with ...[more]

PMID: 20048066

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Project description:The adaptation of bacteria involved in anaerobic ammonium oxidation (anammox) to low temperatures will enable more efficient removal of nitrogen from sewage across seasons. At lower temperatures, bacteria typically tune the synthesis of their membrane lipids to promote membrane fluidity. However, such adaptation of anammox bacteria lipids, including unique ladderane phospholipids and especially shorter ladderanes with absent phosphatidyl headgroup, is yet to be described in detail. We investigated the membrane lipids composition (UPLC-HRMS/MS) and dominant anammox populations (16S rRNA gene amplicon sequencing, Fluorescence in situ hybridization) in 14 anammox enrichments cultivated at 10-37 °C. "Candidatus Brocadia" appeared to be the dominant organism in all but two laboratory enrichments of "Ca. Scalindua" and "Ca. Kuenenia". At lower temperatures, the membranes of all anammox populations were composed of shorter [5]-ladderane ester (reduced chain length demonstrated by decreased fraction of C20/(C18 + C20)). This confirmed the previous preliminary evidence on the prominent role of this ladderane fatty acid in low-temperature adaptation. "Ca. Scalindua" and "Ca. Kuenenia" had distinct profile of ladderane lipids compared to "Ca. Brocadia" biomasses with potential implications for adaptability to low temperatures. "Ca. Brocadia" membranes contained a much lower amount of C18 [5]-ladderane esters than reported in the literature for "Ca. Scalindua" at similar temperature and measured here, suggesting that this could be one of the reasons for the dominance of "Ca. Scalindua" in cold marine environments. Furthermore, we propose additional and yet unreported mechanisms for low-temperature adaptation of anammox bacteria, one of which involves ladderanes with absent phosphatidyl headgroup. In sum, we deepen the understanding of cold anammox physiology by providing for the first time a consistent comparison of anammox-based communities across multiple environments.

Project description:Ladderanes are hydrocarbon chains with three or five linearly concatenated cyclobutane rings that are uniquely produced as membrane lipid components by anammox (anaerobic ammonia-oxidizing) bacteria. By virtue of their angle and torsional strain, ladderanes are unusually energetic compounds, and if produced biochemically by engineered microbes, could serve as renewable, high-energy-density jet fuel components. The biochemistry and genetics underlying the ladderane biosynthetic pathway are unknown, however, previous studies have identified a pool of 34 candidate genes from the anammox bacterium, Kuenenia stuttgartiensis, some or all of which may be involved with ladderane fatty acid biosynthesis. The goal of the present study was to establish a systematic means of testing the candidate genes from K. stuttgartiensis for involvement in ladderane biosynthesis through heterologous expression in E. coli under anaerobic conditions. This study describes an efficient means of assembly of synthesized, codon-optimized candidate ladderane biosynthesis genes in synthetic operons that allows for changes to regulatory element sequences, as well as modular assembly of multiple operons for simultaneous heterologous expression in E. coli (or potentially other microbial hosts). We also describe in vivo functional tests of putative anammox homologs of the phytoene desaturase CrtI, which plays an important role in the hypothesized ladderane pathway, and a method for soluble purification of one of these enzymes. This study is, to our knowledge, the first experimental effort focusing on the role of specific anammox genes in the production of ladderanes, and lays the foundation for future efforts toward determination of the ladderane biosynthetic pathway. Our substantial, but far from comprehensive, efforts at elucidating the ladderane biosynthetic pathway were not successful. We invite the scientific community to take advantage of the considerable synthetic biology resources and experimental results developed in this study to elucidate the biosynthetic pathway that produces unique and intriguing ladderane lipids.

Project description:The discovery of anaerobic ammonia oxidation (anammox) expanded our knowledge on the microbial nitrogen cycle. Previous studies report that anammox bacteria are distributed in a wide range of habitats and plays significant roles in the global nitrogen cycle. However, most studies focus only on individual ecosystems or datasets from public databases. To date, our understanding of how anammox bacteria respond to environmental properties and are distributed in different habitats on a global scale, remain unclear. To explore the global distribution of anammox bacteria, samples were collected from different habitats at different locations globally, including wetlands, drylands, groundwater aquifers and snow from 10 countries across six continents. We then used high-throughput amplicon sequencing targeting the functional gene hydrazine synthase (HZS) and generated community profiles. Results showed that Candidatus Brocadia is detected as the dominant genus on a global scale, accounting for 80.0% to 99.9% of the retrieved sequences in different habitats. The Jettenia-like sequences were the second most abundant group, accounting for no more than 19.9% of the retrieved sequences in all sites. The samples in drylands, wetlands and groundwater aquifers showed similar community composition and diversity, with the snow samples being the most different. Deterministic processes seem stronger in regulating the community composition of anammox bacteria, which is supported by the higher proportion explained by local-scale factors. Groundwater aquifers showed high gene abundance and the most complex co-occurrence network among the four habitat types, suggesting that it might be the preferred habitat of anammox bacteria. There is little competition between anammox bacterial species based on co-occurrence analysis. Hence, we could infer that environmental factors such as anaerobic and stable conditions, instead of substrate limitations, may be vital factors determining the anammox bacteria community. These results provide a better understanding of the global distribution of anammox bacteria and the ecological factors that affect their community structuring in diverse habitats.

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Impact of temperature on ladderane lipid distribution in anammox bacteria.

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Impact of temperature on ladderane lipid distribution in anammox bacteria.

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