Physiological, chemotaxonomic and genomic characterization of two novel piezotolerant bacteria of the family Marinifilaceae isolated from sulfidic waters of the Black Sea

Yadav, Subhash; Villanueva, Laura; Bale, Nicole J.; Koenen, Michel; Hopmans, Ellen C.; Damsté, Jaap S. Sinninghe

doi:10.1016/j.syapm.2020.126122

Cited by 16 publications

(45 citation statements)

References 62 publications

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“…in the Black Sea water column. Data were obtained by sampling with Niskin bottles, filtration, DNA extraction, 16S rRNA gene amplicon sequencing and quantitative PCR, both using the same universal bacterial primers (see Yadav et al ., 2020; Villanueva et al ., 2021). Note that the depth axis in (A) and (B) is not to scale.…”

Section: Resultsmentioning

confidence: 99%

“…In this study, we have examined the distribution and abundance of fusobacterial members in the Black Sea water column. The Black Sea is the largest permanent anoxic basin on Earth, with a maximum depth of approximately 2200 m. The Black Sea deep waters (>2000 m) are characterized recalcitrant nutrient conditions (i.e., the presence of difficult to degrade sulfurized dissolved organic matters; Gomez-Saez et al, 2021), elevated hydrostatic pressure and high sulfide concentration (400 μM; Volkov and Neretin, 2007), conditions that are expected to harbour microorganisms adapted to deal with those conditions (e.g., Vetriani et al, 2003;Wakeham et al, 2003Wakeham et al, , 2007Lin et al, 2006;Leloup et al, 2007;Henkel et al, 2019;Yadav et al, 2020;Suominen et al, 2021aSuominen et al, , 2021b. Here, we have successfully enriched members of the genus Psychrilyobacter (up to 58% of the total microbial community) of the phylum Fusobacteria and isolated two representative strains (Psychrilyobacter sp.…”

Section: Introductionmentioning

confidence: 99%

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The physiology and metabolic properties of a novel, low‐abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role

Yadav

Koenen

Bale

et al. 2021

Environ Microbiol Rep

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Members of the Psychrilyobacter spp. of the phylum Fusobacteria have been recently suggested to be amongst the most significant primary degraders of the detrital organic matter in sulfidic marine habitats, despite representing only a small proportion (<0.1%) of the microbial community. In this study, we have isolated a previously uncultured Psychrilyobacter species (strains SD5 T and BL5; Psychrilyobacter piezotolerans sp. nov.) from the sulfidic waters (i.e., 2000 m depth) of the Black Sea and investigated its physiology and genomic capability in order to better understand potential ecological adaptation strategies. P. piezotolerans utilized a broad range of organic substituents (carbohydrates and proteins) and, remarkably, grew at sulfide concentrations up to 32 mM. These flexible physiological properties were supported by the presence of the respective metabolic pathways in the genomes of both strains. Growth at varying hydrostatic pressure (0.1-50 MPa) was sustained by modifying its membrane lipid composition. Thus, we have isolated a novel member of the 'rare biosphere', which endures the extreme conditions and may play a significant role in the degradation of detrital organic matter sinking into the sulfidic waters of the Black Sea.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The physiology and metabolic properties of a novel, low‐abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role

Yadav

Koenen

Bale

et al. 2021

Environ Microbiol Rep

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“…nov. Labilibaculum euxinus sp. nov., and Lutibacter sp., all isolated from the euxinic zone of the Black Sea, were found to have capnines among their most abundant lipids ( Bale et al, 2020 ; Yadav et al, 2020 ). Capnines were also found in the molecular network ( Figure 2 ).…”

Section: Resultsmentioning

confidence: 99%

Lipidomics of Environmental Microbial Communities. II: Characterization Using Molecular Networking and Information Theory

et al. 2021

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Structurally diverse, specialized lipids are crucial components of microbial membranes and other organelles and play essential roles in ecological functioning. The detection of such lipids in the environment can reveal not only the occurrence of specific microbes but also the physicochemical conditions to which they are adapted to. Traditionally, liquid chromatography coupled with mass spectrometry allowed for the detection of lipids based on chromatographic separation and individual peak identification, resulting in a limited data acquisition and targeting of certain lipid groups. Here, we explored a comprehensive profiling of microbial lipids throughout the water column of a marine euxinic basin (Black Sea) using ultra high-pressure liquid chromatography coupled with high-resolution tandem mass spectrometry (UHPLC-HRMS/MS). An information theory framework combined with molecular networking based on the similarity of the mass spectra of lipids enabled us to capture lipidomic diversity and specificity in the environment, identify novel lipids, differentiate microbial sources within a lipid group, and discover potential biomarkers for biogeochemical processes. The workflow presented here allows microbial ecologists and biogeochemists to process quickly and efficiently vast amounts of lipidome data to understand microbial lipids characteristics in ecosystems.

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“…Diether lipids have been detected in a limited number of bacteria (e.g., Grossi et al, 2015) but their (core lipid) abundance in the Black Sea water column has been shown to correlate with sulfate reducing bacteria (SRB; Neretin et al, 2007). Two components, tentatively assigned as sulfate-1-deoxyceramides (Ding et al, 2021), were also among most abundant components in cluster D. Ding et al (2021) hypothesize that, as bacterial sphingolipids are mainly produced by Bacteroidetes and selected Proteobacteria (Heaver et al, 2018) and because certain Bacteroidetes from the Black Sea are known to produce capnines (Bale et al, 2020;Yadav et al, 2020), sulfonoanalogs of sphinganine (Godchaux and Leadbetter, 1980), that these novel sulfate-1-deoxyceramides, may also be produced by anaerobic heterotrophs related to Bacteroidetes.…”

Section: Abundant Components In Major Clustersmentioning

confidence: 99%

Lipidomics of Environmental Microbial Communities. I: Visualization of Component Distributions Using Untargeted Analysis of High-Resolution Mass Spectrometry Data

et al. 2021

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Lipids, as one of the main building blocks of cells, can provide valuable information on microorganisms in the environment. Traditionally, gas or liquid chromatography coupled to mass spectrometry (MS) has been used to analyze environmental lipids. The resulting spectra were then processed through individual peak identification and comparison with previously published mass spectra. Here, we present an untargeted analysis of MS1 spectral data generated by ultra-high-pressure liquid chromatography coupled with high-resolution mass spectrometry of environmental microbial communities. Rather than attempting to relate each mass spectrum to a specific compound, we have treated each mass spectrum as a component, which can be clustered together with other components based on similarity in their abundance depth profiles through the water column. We present this untargeted data visualization method on lipids of suspended particles from the water column of the Black Sea, which included >14,000 components. These components form clusters that correspond with distinct microbial communities driven by the highly stratified water column. The clusters include both known and unknown compounds, predominantly lipids, demonstrating the value of this rapid approach to visualize component distributions and identify novel lipid biomarkers.

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Physiological, chemotaxonomic and genomic characterization of two novel piezotolerant bacteria of the family Marinifilaceae isolated from sulfidic waters of the Black Sea

Cited by 16 publications

References 62 publications

The physiology and metabolic properties of a novel, low‐abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role

The physiology and metabolic properties of a novel, low‐abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role

Lipidomics of Environmental Microbial Communities. II: Characterization Using Molecular Networking and Information Theory

Lipidomics of Environmental Microbial Communities. I: Visualization of Component Distributions Using Untargeted Analysis of High-Resolution Mass Spectrometry Data

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