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Effect of temperature on the compositions of ladderane lipids in globally surveyed anammox populations.

ABSTRACT: 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.

SUBMITTER: Kouba V

PROVIDER: S-EPMC7612979 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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:Bacteria specialized in anaerobic ammonium oxidation (anammox) are widespread in many anoxic habitats and form an important functional guild in the global nitrogen cycle by consuming bio-available nitrogen for energy rather than biomass production. Due to their slow growth rates, cultivation-independent approaches have been used to decipher their diversity across environments. However, their full diversity has not been well recognized. Here, we report a new family of putative anammox bacteria, "Candidatus Subterrananammoxibiaceae," existing in the globally distributed terrestrial and marine subsurface (groundwater and sediments of estuary, deep-sea, and hadal trenches). We recovered a high-quality metagenome-assembled genome of this family, tentatively named "Candidatus Subterrananammoxibius californiae," from a California groundwater site. The "Ca. Subterrananammoxibius californiae" genome not only contains genes for all essential components of anammox metabolism (e.g., hydrazine synthase, hydrazine oxidoreductase, nitrite reductase, and nitrite oxidoreductase) but also has the capacity for urea hydrolysis. In an Arctic ridge sediment core where redox zonation is well resolved, "Ca. Subterrananammoxibiaceae" is confined within the nitrate-ammonium transition zone where the anammox rate maximum occurs, providing environmental proof of the anammox activity of this new family. Phylogenetic analysis of nitrite oxidoreductase suggests that a horizontal transfer facilitated the spreading of the nitrite oxidation capacity between anammox bacteria (in the Planctomycetota phylum) and nitrite-oxidizing bacteria from Nitrospirota and Nitrospinota. By recognizing this new anammox family, we propose that all lineages within the "Ca. Brocadiales" order have anammox capacity. IMPORTANCE Microorganisms called anammox bacteria are efficient in removing bioavailable nitrogen from many natural and human-made environments. They exist in almost every anoxic habitat where both ammonium and nitrate/nitrite are present. However, only a few anammox bacteria have been cultured in laboratory settings, and their full phylogenetic diversity has not been recognized. Here, we present a new bacterial family whose members are present across both the terrestrial and marine subsurface. By reconstructing a high-quality genome from the groundwater environment, we demonstrate that this family has all critical enzymes of anammox metabolism and, notably, also urea utilization. This bacterium family in marine sediments is also preferably present in the niche where the anammox process occurs. These findings suggest that this novel family, named "Candidatus Subterrananammoxibiaceae," is an overlooked group of anammox bacteria, which should have impacts on nitrogen cycling in a range of environments.

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Effect of temperature on the compositions of ladderane lipids in globally surveyed anammox populations.

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