Distribution and Genomic Variation of Thermophilic Cyanobacteria in Diverse Microbial Mats at the Upper Temperature Limits of Photosynthesis

Kees, Eric D.; Murugapiran, Senthil K.; Bennett, Annastacia C.; Hamilton, Trinity L.

doi:10.1128/msystems.00317-22

Cited by 19 publications

(16 citation statements)

References 88 publications

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“…Waters that reside deeper in the subsurface receive minimal meteoric water input and therefore have less influence from heterogeneous shallow subsurface geology and precipitation variability ( Fournier, 1989 ). As the hydrothermal waters cool along the SC outflow from 0 to 1 m, a major temperature threshold was crossed [72/73°C, the upper limit of photosynthesis, ( Brock, 1978 ; Kees et al, 2022 )] allowing for the proliferation of phototrophs such as Leptococcus and Geitlerinema . Such a major shift in detectable microbial communities indicates that temperature is critical in the establishment of fundamental niches at SC, a precedent previously established at other biomat locations ( Wang et al, 2013 ; Bennett et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Spatial and temporal dynamics at an actively silicifying hydrothermal system

et al. 2023

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Steep Cone Geyser is a unique geothermal feature in Yellowstone National Park (YNP), Wyoming, actively gushing silicon-rich fluids along outflow channels possessing living and actively silicifying microbial biomats. To assess the geomicrobial dynamics occurring temporally and spatially at Steep Cone, samples were collected at discrete locations along one of Steep Cone’s outflow channels for both microbial community composition and aqueous geochemistry analysis during field campaigns in 2010, 2018, 2019, and 2020. Geochemical analysis characterized Steep Cone as an oligotrophic, surface boiling, silicious, alkaline-chloride thermal feature with consistent dissolved inorganic carbon and total sulfur concentrations down the outflow channel ranging from 4.59 ± 0.11 to 4.26 ± 0.07 mM and 189.7 ± 7.2 to 204.7 ± 3.55 μM, respectively. Furthermore, geochemistry remained relatively stable temporally with consistently detectable analytes displaying a relative standard deviation <32%. A thermal gradient decrease of ~55°C was observed from the sampled hydrothermal source to the end of the sampled outflow transect (90.34°C ± 3.38 to 35.06°C ± 7.24). The thermal gradient led to temperature-driven divergence and stratification of the microbial community along the outflow channel. The hyperthermophile Thermocrinis dominates the hydrothermal source biofilm community, and the thermophiles Meiothermus and Leptococcus dominate along the outflow before finally giving way to more diverse and even microbial communities at the end of the transect. Beyond the hydrothermal source, phototrophic taxa such as Leptococcus, Chloroflexus, and Chloracidobacterium act as primary producers for the system, supporting heterotrophic growth of taxa such as Raineya, Tepidimonas, and Meiothermus. Community dynamics illustrate large changes yearly driven by abundance shifts of the dominant taxa in the system. Results indicate Steep Cone possesses dynamic outflow microbial communities despite stable geochemistry. These findings improve our understanding of thermal geomicrobiological dynamics and inform how we can interpret the silicified rock record.

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Section: Discussionmentioning

confidence: 99%

Spatial and temporal dynamics at an actively silicifying hydrothermal system

et al. 2023

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“…Waters that reside deeper in the subsurface receive minimal meteoric water input and therefore have less influence from heterogeneous shallow subsurface geology and precipitation variability (Fournier, 1989). As the hydrothermal waters cool along the SC outflow from 0 to 1 m, a major temperature threshold was crossed (72/73°C, the upper limit of photosynthesis, (Brock, 1978; Kees et al, 2022)) allowing for the proliferation of phototrophs such as Leptococcus and Geitlerinema . Such a major shift in detectable microbial communities indicates that temperature is critical in the establishment of fundamental niches at SC, a precedent previously established at other biomat locations (Bennett et al, 2020; Wang et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Spatial and Temporal Dynamics at an Actively Silicifying Hydrothermal System

Rasmussen

Stamps

Vanzin

et al. 2023

Preprint

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Steep Cone Geyser is a unique geothermal feature in Yellowstone National Park, Wyoming (YNP), actively gushing silicon rich fluids along outflow channels possessing living and actively silicifying microbial biomats. To assess the geomicrobial dynamics occurring temporally and spatially at Steep Cone, samples were collected at discrete locations along one of Steep Cones outflow channels for both microbial community composition and aqueous geochemistry analysis during field campaigns in 2010, 2018, 2019, and 2020. Geochemical analysis characterized Steep Cone as an oligotrophic, surface boiling, silicious, alkaline-chloride thermal feature with consistent dissolved inorganic carbon and total sulfur concentrations down the outflow channel ranging from 4.59 +/- 0.11 to 4.26 +/- 0.07 mM and 189.7 +/- 7.2 to 204.7 +/- 3.55 uM respectively. Furthermore, geochemistry remained relatively stable temporally with consistently detectable analytes displaying a relative standard deviation < 32%. A thermal gradient decrease of ~55C was observed from the sampled hydrothermal source to the end of the sampled outflow transect (90.34C +/- 3.38 to 35.06C +/- 7.24). The thermal gradient led to temperature-driven divergence and stratification of the microbial community along the outflow channel. The hyperthermophile Thermocrinis dominates the hydrothermal source biofilm community, and the thermophiles Meiothermus and Leptococcus dominate along the outflow before finally giving way to more diverse and even microbial communities at the end of the transect. Beyond the hydrothermal source, phototrophic taxa such as Leptococcus, Chloroflexus, and Chloracidobacterium act as primary producers for the system supporting heterotrophic growth of taxa such as Raineya, Tepidimonas, and Meiothermus. Community dynamics illustrate large changes yearly driven by abundance changes of the dominant taxa in the system. Results indicate Steep Cone possesses dynamic outflow microbial communities despite stable geochemistry. These findings improve our understanding of thermal geomicrobiological dynamics and inform how we can interpret the silicified rock record.

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“…Pchlide reduction has endured various selective pressures across a range of environmental parameters after the transition of photosynthesis from an initial anoxygenic to an oxygenic environment. Some of the environmental factors include a) High altitude, b) Fe deficiency and c) high temperature, d) light intensity, e) light quality (Li and Bridwell-Rabb, 2018;Przybyla-Toscano et al, 2021;Abbas et al, 2022;Kees et al, 2022).…”

Section: Impact Of Other Environmental Factors On Lpor Origin and Evo...mentioning

confidence: 99%

“…Although cyanobacteria mostly possess both the Pchlide reducing enzymes i.e., LIPOR and LPOR; thermophilic cyanobacteria lack both LIPOR genes and nitrogenase genes. This loss of LIPOR genes is attributed to high temperature-induced genome reduction in thermophilic cyanobacteria (Kees et al, 2022).…”

Section: Impact Of Other Environmental Factors On Lpor Origin and Evo...mentioning

confidence: 99%

Fortuitous events in the evolution of Light-dependent Protochlorophyllide Oxidoreductase

Vedalankar

Tripathy

2023

Preprint

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Light-dependent protochlorophyllide oxidoreductase (LPOR) is a nuclear-encoded photoenzyme in many photosynthetic organisms. LPOR originated in primitive cyanobacterial ancestors during the great oxygenation event that was detrimental to the existence of the oxygen-sensitive LIPOR that prevailed in anoxygenic Earth. Both LIPOR and LPOR catalyse reduction of protochlorophyllide to chlorophyllide in the penultimate step of chlorophyll biosynthesis. Except for angiosperms and gnetophytes several oxygenic phototrophs harbour both LIPOR and LPOR. The coexistence of LIPOR and LPOR in certain phototrophs provides niche spaces for organisms in unconducive environment. The selection pressure of increased O2 concentration, changing light quality and quantity at different depths of the ocean, nutrient status of water, gene reorganization during several endosymbiotic events, horizontal gene transfer, LIPOR gene loss and multiple duplication events played a major role in the evolution and diversification of LPOR and its isoforms in photosynthetic and non-photosynthetic organisms. In the absence of LIPOR angiosperms become vulnerable to protochlorophyllide-sensitized and light-induced oxidative stress mediated by singlet oxygen. To overcome the photo-damage PORA was expressed abundantly in the plastids of etiolated plants. PORB evolved to take over the function of vanishing PORA isoform in light. Brassicales evolved PORC to protect plants from high light and other environmental stresses.

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Distribution and Genomic Variation of Thermophilic Cyanobacteria in Diverse Microbial Mats at the Upper Temperature Limits of Photosynthesis

Cited by 19 publications

References 88 publications

Spatial and temporal dynamics at an actively silicifying hydrothermal system

Spatial and temporal dynamics at an actively silicifying hydrothermal system

Spatial and Temporal Dynamics at an Actively Silicifying Hydrothermal System

Fortuitous events in the evolution of Light-dependent Protochlorophyllide Oxidoreductase

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