Dataset Information

Validation of a Hypothesis: Colonization of Black Smokers by Hyperthermophilic Microorganisms.

ABSTRACT: Newly erupted black smokers (hydrothermal vent chimneys) are sterile during their formation, but house hyperthermophilic microorganisms in substantial amounts in later stages. No direct experimental data exist by which mechanisms hyperthermophiles colonize newly erupted black smokers, but a scenario was proposed recently how this might happen. Here we combine high temperature light microscopy with electron microscopy to show that two hyperthermophilic Archaea, namely Pyrococcus furiosus and Methanocaldococcus villosus are able to adhere onto authentic black smoker material (BSM). We especially are able to directly observe the adhesion process via video recordings taken at high temperatures. These data validate the hypothesis that hyperthermophiles are transferred by serendipitous water currents to the outside of newly formed black smokers and react within seconds to the there prevailing high temperatures by very fast movements. They scan the surface of the hydrothermal chimneys via a much slower zigzag seek-movement and adhere via their flagella at a suitable place, building up biofilms.

SUBMITTER: Wirth R

PROVIDER: S-EPMC5871681 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Validation of a Hypothesis: Colonization of Black Smokers by Hyperthermophilic Microorganisms.

Wirth Reinhard R Luckner Manja M Wanner Gerhard G

Frontiers in microbiology 20180321

Newly erupted black smokers (hydrothermal vent chimneys) are sterile during their formation, but house hyperthermophilic microorganisms in substantial amounts in later stages. No direct experimental data exist by which mechanisms hyperthermophiles colonize newly erupted black smokers, but a scenario was proposed recently how this might happen. Here we combine high temperature light microscopy with electron microscopy to show that two hyperthermophilic Archaea, namely <i>Pyrococcus furiosus and M ...[more]

PMID: 29619021

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Project description:Biological activity at deep-sea hydrothermal chimneys is driven by chemotrophic microorganisms that metabolize chemicals from the venting high-temperature fluids. Understanding taphonomy and microbial microtextures in such environments is a necessity for micropaleontological and palaeoecological research. This study examines fossilized microorganisms and related microtextures in a recent black smoker from the Roman Ruins hydrothermal vent site, Eastern Manus Basin offshore of Papua New Guinea. Whereas the center of the examined sulfide chimney is dominated by high-temperature mineralogy (chalcopyrite and dendritic sphalerite), filamentous and coccoidal biomorphs occur in an outer, warm zone of mixing between hydrothermal fluids and seawater, which is indicated by their occurrence within colloform and botryoidal pyrite of barite-pyrite coprecipitates. Both morphotypes can be interpreted as thermophilic microorganisms based on their occurrence in a high-temperature habitat. Their separate (non-commensal) occurrence hints at sensitivities to microenvironmental conditions, which is expectable for strong temperature, pH, and redox gradients at the walls of deep-sea hydrothermal chimneys. Whereas both morphotypes experienced mild thermal overprint, taphonomic differences exist: (i) spaces left by cells in filamentous fossils are predominately filled by silica, whereas inter/extracellular features (crosswalls/septae and outer sheaths) are pyritized; (ii) coccoidal fossils show both silica- and pyrite-infilled interiors, and generally better preservation of cell walls. These different manifestations presumably relate to an interplay between microenvironmental and biological factors, potentially contrasting metabolisms, and differences in cell wall chemistries of distinct bacteria and/or archaea. A further hypothesis is that the coccoidal features represent biofilm-forming organisms, whose organic matter derivates contributed to the formation of intimately associated wavy and wrinkly carbonaceous laminations that are at least locally distinguishable from the texture of the surrounding pyrite. Hence, the presented data provide evidence that microtextures of microbiota from hydrothermal systems can have a similar significance for palaeobiological research as those from sedimentary environments.

Project description:Industrial biomining processes are currently focused on metal sulfides and their dissolution, which is catalyzed by acidophilic iron(II)- and/or sulfur-oxidizing microorganisms. Cell attachment on metal sulfides is important for this process. Biofilm formation is necessary for seeding and persistence of the active microbial community in industrial biomining heaps and tank reactors, and it enhances metal release. In this study, we used a method for direct quantification of the mineral-attached cell population on pyrite or chalcopyrite particles in bioleaching experiments by coupling high-throughput, automated epifluorescence microscopy imaging of mineral particles with algorithms for image analysis and cell quantification, thus avoiding human bias in cell counting. The method was validated by quantifying cell attachment on pyrite and chalcopyrite surfaces with axenic cultures of Acidithiobacillus caldus, Leptospirillum ferriphilum, and Sulfobacillus thermosulfidooxidans. The method confirmed the high affinity of L. ferriphilum cells to colonize pyrite and chalcopyrite surfaces and indicated that biofilm dispersal occurs in mature pyrite batch cultures of this species. Deep neural networks were also applied to analyze biofilms of different microbial consortia. Recent analysis of the L. ferriphilum genome revealed the presence of a diffusible soluble factor (DSF) family quorum sensing system. The respective signal compounds are known as biofilm dispersal agents. Biofilm dispersal was confirmed to occur in batch cultures of L. ferriphilum and S. thermosulfidooxidans upon the addition of DSF family signal compounds.IMPORTANCE The presented method for the assessment of mineral colonization allows accurate relative comparisons of the microbial colonization of metal sulfide concentrate particles in a time-resolved manner. Quantitative assessment of the mineral colonization development is important for the compilation of improved mathematical models for metal sulfide dissolution. In addition, deep-learning algorithms proved that axenic or mixed cultures of the three species exhibited characteristic biofilm patterns and predicted the biofilm species composition. The method may be extended to the assessment of microbial colonization on other solid particles and may serve in the optimization of bioleaching processes in laboratory scale experiments with industrially relevant metal sulfide concentrates. Furthermore, the method was used to demonstrate that DSF quorum sensing signals directly influence colonization and dissolution of metal sulfides by mineral-oxidizing bacteria, such as L. ferriphilum and S. thermosulfidooxidans.

Dataset Information

Validation of a Hypothesis: Colonization of Black Smokers by Hyperthermophilic Microorganisms.

Publications

Validation of a Hypothesis: Colonization of Black Smokers by Hyperthermophilic Microorganisms.

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