Genome-resolved Metagenomics and Metatranscriptomics Reveal Niche Differentiation in Functionally Redundant Microbial Communities at Deep-sea Hydrothermal Vents (Environmental Microbiology, 2019)

The structure and function of microbial communities inhabiting the subseafloor near hydrothermal systems are influenced by fluid geochemistry, geologic setting and fluid flux between vent sites, as well as biological interactions. Here, we used genome?resolved metagenomics and metatranscriptomics to examine patterns of gene abundance and expression and assess potential niche differentiation in microbial communities in venting fluids from hydrothermal vent sites at the Mid?Cayman Rise. We observed similar patterns in gene and transcript abundance between two geochemically distinct vent fields at the community level but found that each vent site harbours a distinct microbial community with differing transcript abundances for individual microbial populations. Through an analysis of metabolic pathways in 64 metagenome?assembled genomes (MAGs), we show that MAG transcript abundance can be tied to differences in metabolic pathways and to potential metabolic interactions between microbial populations, allowing for niche?partitioning and divergence in both population distribution and activity. Our results illustrate that most microbial populations have a restricted distribution within the seafloor, and that the activity of those microbial populations is tied to both genome content and abiotic factors.

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Does the Evolution of Complex Life Depend on the Stellar Spectral Energy Distribution? (Astrobiology, 2019)

This article presents the proportional evolutionary time (PET) hypothesis, which posits that the mean time required for the evolution of complex life is a function of stellar mass. The “biological available window” is defined as the region of a stellar spectrum between 200 and 1200?nm that generates free energy for life. Over the ?4 Gyr history of Earth, the total energy incident at the top of the atmosphere and within the biological available window is ?1034 J. The hypothesis assumes that the rate of evolution from the origin of life to complex life is proportional to this total energy, which would suggest that planets orbiting other stars should not show signs of complex life if the total energy incident on the planet is below this energy threshold. The PET hypothesis predicts that late K- and M-dwarf stars (M??0.7 ) represent the best targets for the next generation of space telescopes to search for spectroscopic biosignatures indicative of complex life.

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Statistical Analysis of Curiosity Data Shows No Evidence for a Strong Seasonal Cycle of Martian Methane (Icarus, 2020)

Using Gaussian process regression to analyze the Martian surface methane Tunable Laser Spectrometer (TLS) data reported by Webster et al. (2018), we find that the TLS data, taken as a whole, do not indicate seasonal variability. Enrichment protocol CH4 data are consistent with either stochastic variation or a spread of periods without seasonal preference.

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A Limited Habitable Zone for Complex Life (The Astrophysical Journal, 2019)

The habitable zone (HZ) is commonly defined as the range of distances from a host star within which liquid water, a key requirement for life, may exist on a planet’s surface. Substantially more CO2 than present in Earth’s modern atmosphere is required to maintain clement temperatures for most of the HZ, with several bars required at the outer edge. However, most complex aerobic life on Earth is limited by CO2 concentrations of just fractions of a bar. At the same time, most exoplanets in the traditional HZ reside in proximity to M dwarfs, which are more numerous than Sun-like G dwarfs but are predicted to promote greater abundances of gases that can be toxic in the atmospheres of orbiting planets, such as carbon monoxide (CO). Here we show that the HZ for complex aerobic life is likely limited relative to that for microbial life. We use a 1D radiative-convective climate and photochemical models to circumscribe a Habitable Zone for Complex Life (HZCL) based on known toxicity limits for a range of organisms as a proof of concept. We find that for CO2 tolerances of 0.01, 0.1, and 1 bar, the HZCL is only 21%, 32%, and 50% as wide as the conventional HZ for a Sun-like star, and that CO concentrations may limit some complex life throughout the entire HZ of the coolest M dwarfs. These results cast new light on the likely distribution of complex life in the universe and have important ramifications for the search for exoplanet biosignatures and technosignatures.

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Rethinking CO Antibiosignatures in the Search for Life Beyond the Solar System (The Astrophysical Journal, 2019)

Some atmospheric gases have been proposed as counter indicators to the presence of life on an exoplanet if remotely detectable at sufficient abundance (i.e., antibiosignatures), informing the search for biosignatures and potentially fingerprinting uninhabited habitats. However, the quantitative extent to which putative antibiosignatures could exist in the atmospheres of inhabited planets is not well understood. The most commonly referenced potential antibiosignature is CO, because it represents a source of free energy and reduced carbon that is readily exploited by life on Earth and is thus often assumed to accumulate only in the absence of life. Yet, biospheres actively produce CO through biomass burning, photooxidation processes, and release of gases that are photochemically converted into CO in the atmosphere. We demonstrate with a 1D ecosphere-atmosphere model that reducing biospheres can maintain CO levels of ~100 ppmv even at low H2 fluxes due to the impact of hybrid photosynthetic ecosystems. Additionally, we show that photochemistry around M dwarf stars is particularly favorable for the buildup of CO, with plausible concentrations for inhabited, oxygen-rich planets extending from hundreds of ppm to several percent. Since CH4 buildup is also favored on these worlds, and because O2 and O3 are likely not detectable with the James Webb Space Telescope, the presence of high CO (>100 ppmv) may discriminate between oxygen-rich and reducing biospheres with near-future transmission observations. These results suggest that spectroscopic detection of CO can be compatible with the presence of life and that a comprehensive contextual assessment is required to validate the significance of potential antibiosignatures.

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The K Dwarf Advantage for Biosignatures on Directly Imaged Exoplanets (The Astrophysical Journal, 2019)

Oxygen and methane are considered to be the canonical biosignatures of modern Earth, and the simultaneous detection of these gases in a planetary atmosphere is an especially strong biosignature. However, these gases may be challenging to detect together in the planetary atmospheres because photochemical oxygen radicals destroy methane. Previous work has shown that the photochemical lifetime of methane in oxygenated atmospheres is longer around M dwarfs, but M dwarf planet habitability may be hindered by extreme stellar activity and evolution. Here, we use a 1D photochemical-climate model to show that K dwarf stars also offer a longer photochemical lifetime of methane in the presence of oxygen compared to G dwarfs. For example, we show that a planet orbiting a K6V star can support about an order of magnitude more methane in its atmosphere compared to an equivalent planet orbiting a G2V star. In the reflected-light spectra of worlds orbiting K dwarf stars, strong oxygen and methane features could be observed at visible and near-infrared wavelengths. Because K dwarfs are dimmer than G dwarfs, they offer a better planet-star contrast ratio, enhancing the signal-to-noise ratio (S/N) possible in a given observation. For instance, a 50 hr observation of a planet at 7 pc with a 15 m telescope yields S/N = 9.2 near 1 ?m for a planet orbiting a solar-type G2V star, and S/N = 20 for the same planet orbiting a K6V star. In particular, nearby mid-late K dwarfs such as 61 Cyg A/B, Epsilon Indi, Groombridge 1618, and HD 156026 may be excellent targets for future biosignature searches.

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Astrobiology: A Very Short Introduction (Oxford University Press, 2014)

What fascinates people about astrobiology is that it seeks answers to long-standing unsolved questions: How quickly did life evolve on Earth and why did life persist here? Is there life elsewhere in the Solar System or beyond? Astrobiology: A Very Short Introduction explores some of the big unanswered questions about the universe, considers the origins of life on Earth and its evolution, and brings together the ideas of microbiologists, astronomers, planetary scientists, and geologists. It introduces the origins of astrobiology and demonstrates its impact on current astronomical research and…

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Characterizing the purple Earth: Modelling the globally-integrated spectral variability of the Archean Earth (The Astrophysical Journal, 2013)

The ongoing searches for exoplanetary systems have revealed a wealth of planets with diverse physical properties. Planets even smaller than the Earth have already been detected, and the efforts of future missions are placed on the discovery, and perhaps characterization, of small rocky exoplanets within the habitable zone of their stars. Clearly what we know about our planet will be our guideline for the characterization of such planets. But the Earth has been inhabited for at least 3.8 Ga, and its appearance has changed with time. Here, we have studied the Earth during the Archean eon, 3.0 Ga ago. At that time one of the more widespread life forms on the planet were purple bacteria. These bacteria are photosynthetic microorganisms and can inhabit both aquatic and terrestrial environments. Here, we used a radiative transfer model to simulate the visible and near-IR radiation reflected by our planet, taking into account several scenarios regarding the possible distribution of purple bacteria over continents and oceans. We find that purple bacteria have a reflectance spectrum which has a strong reflectivity increase, similar to the red edge of leafy plants, although shifted redwards. This feature produces a detectable signal in the disk-averaged spectra of our planet, depending on cloud amount and on purple bacteria concentration/distribution. We conclude that by using multi-color photometric observations, it is possible to distinguish between an Archean Earth in which purple bacteria inhabit vast extensions of the planet, and a present-day Earth with continents covered by deserts, vegetation or microbial mats.

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Nucleobases bind to and stabilize aggregates of a prebiotic amphiphile, providing a viable mechanism for the emergence of protocells (PNAS, 2013)

Primordial cells presumably combined RNAs, which functioned as catalysts and carriers of genetic information, with an encapsulating membrane of aggregated amphiphilic molecules. Major questions regarding this hypothesis include how the four bases and the sugar in RNA were selected from a mixture of prebiotic compounds and colocalized with such membranes, and how the membranes were stabilized against flocculation in salt water. To address these questions, we explored the possibility that aggregates of decanoic acid, a prebiotic amphiphile, interact with the bases and sugar found in RNA. We found that these bases, as well as some but not all related bases, bind to decanoic acid aggregates. Moreover, both the bases and ribose inhibit flocculation of decanoic acid by salt. The extent of inhibition by the bases correlates with the extent of their binding, and ribose inhibits to a greater extent than three similar sugars. Finally, the stabilizing effects of a base and ribose are additive. Thus, aggregates of a prebiotic amphiphile bind certain heterocyclic bases and sugars, including those found in RNA, and this binding stabilizes the aggregates against salt. These mutually reinforcing mechanisms might have driven the emergence of protocells.

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Photosystem trap energies and spectrally-dependent energy-storage efficiencies in the Chl d-utilizing cyanobacterium, Acaryochloris marina (BBA Bioenergetics, 2013)

Acaryochloris marina is the only species known to utilize chlorophyll (Chl) d as a principal photopigment. The peak absorption wavelength of Chl d is redshifted ≈40nm in vivo relative to Chl a, enabling this cyanobacterium to perform oxygenic phototrophy in niche environments enhanced in far-red light. We present measurements of the in vivo energy-storage (E-S) efficiency of photosynthesis in A. marina, obtained using pulsed photoacoustics (PA) over a 90-nm range of excitation wavelengths in the red and far-red. Together with modeling results, these measurements provide the first direct observation of the trap energies of PSI and PSII, and also the photosystem-specific contributions to the total E-S efficiency. We find the maximum observed efficiency in A. marina (40±1% at 735nm) is higher than in the Chl a cyanobacterium Synechococcus leopoliensis (35±1% at 690nm). The efficiency at peak absorption wavelength is also higher in A. marina (36±1% at 710nm vs. 31±1% at 670nm). In both species, the trap efficiencies are ≈40% (PSI) and ≈30% (PSII). The PSI trap in A. marina is found to lie at 740±5nm, in agreement with the value inferred from spectroscopic methods. The best fit of the model to the PA data identifies the PSII trap at 723±3nm, supporting the view that the primary electron-donor is Chl d, probably at the accessory (Chl(D1)) site. A decrease in efficiency beyond the trap wavelength, consistent with uphill energy transfer, is clearly observed and fit by the model. These results demonstrate that the E-S efficiency in A. marina is not thermodynamically limited, suggesting that oxygenic photosynthesis is viable in even redder light environments.

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Man and his spaceships: Vehicles for extraterrestrial colonization? (Mobile Genetic Elements, 2012)

The resiliency and adaptive ability of microbial life in real time on Earth relies heavily upon horizontal gene transfer. Based on that knowledge, how likely is earth based microbial life to colonize extraterrestrial targets such as Mars? To address this question, we consider manned and unmanned space exploration, the resident microbiota that is likely to inhabit those vehicles, the adaptive potential of that microbiota in an extraterrestrial setting especially with regards to mobile genetic elements, and the likelihood that Mars like environments could initiate and sustain colonization.

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Is the genetic landscape of the deep subsurface biosphere affected by viruses? (Frontiers in Microbiology, 2011)

Viruses are powerful manipulators of microbial diversity, biogeochemistry, and evolution in the marine environment. Viruses can directly influence the genetic capabilities and the fitness of their hosts through the use of fitness factors and through horizontal gene transfer. However, the impact of viruses on microbial ecology and evolution is often overlooked in studies of the deep subsurface biosphere. Subsurface habitats connected to hydrothermal vent systems are characterized by constant fluid flux, dynamic environmental variability, and high microbial diversity. In such conditions, high adaptability would be an evolutionary asset, and the potential for frequent host–virus interactions would be high, increasing the likelihood that cellular hosts could acquire novel functions. Here, we review evidence supporting this hypothesis, including data indicating that microbial communities in subsurface hydrothermal fluids are exposed to a high rate of viral infection, as well as viral metagenomic data suggesting that the vent viral assemblage is particularly enriched in genes that facilitate horizontal gene transfer and host adaptability. Therefore, viruses are likely to play a crucial role in facilitating adaptability to the extreme conditions of these regions of the deep subsurface biosphere. We also discuss how these results might apply to other regions of the deep subsurface, where the nature of virus–host interactions would be altered, but possibly no less important, compared to more energetic hydrothermal systems.

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Physiological differentiation within a single-species biofilm fueled by serpentinization (mBio, 2011)

Carbonate chimneys at the Lost City hydrothermal field are coated in biofilms dominated by a single phylotype of archaea known as Lost City Methanosarcinales. In this study, we have detected surprising physiological complexity in single-species biofilms, which is typically indicative of multispecies biofilm communities. Multiple cell morphologies were visible within the biofilms by transmission electron microscopy, and some cells contained intracellular membranes that may facilitate methane oxidation. Both methane production and oxidation were detected at 70 to 80°C and pH 9 to 10 in samples containing the single-species biofilms. Both processes were stimulated by the presence of hydrogen (H2), indicating that methane production and oxidation are part of a syntrophic interaction. Metagenomic data included a sequence encoding AMP-forming acetyl coenzyme A synthetase, indicating that acetate may play a role in the methane-cycling syntrophy. A wide range of nitrogen fixation genes were also identified, many of which were likely acquired via lateral gene transfer (LGT). Our results indicate that cells within these single-species biofilms may have differentiated into multiple physiological roles to form multicellular communities linked by metabolic interactions and LGT. Communities similar to these Lost City biofilms are likely to have existed early in the evolution of life, and we discuss how the multicellular characteristics of ancient hydrogen-fueled biofilm communities could have stimulated ecological diversification, as well as unity of biochemistry, during the earliest stages of cellular evolution.

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Using Biogenic Sulfur Gases as Remotely Detectable Biosignatures on Anoxic Planets (Astrobiology, 2011)

We used one-dimensional photochemical and radiative transfer models to study the potential of organic sulfur compounds (CS2, OCS, CH3SH, CH3SCH3, and CH3S2CH3) to act as remotely detectable biosignatures in anoxic exoplanetary atmospheres. Concentrations of organic sulfur gases were predicted for various biogenic sulfur fluxes into anoxic atmospheres and were found to increase with decreasing UV fluxes. Dimethyl sulfide (CH3SCH3, or DMS) and dimethyl disulfide (CH3S2CH3, or DMDS) concentrations could increase to remotely detectable levels, but only in cases of extremely low UV fluxes, which may occur in the habitable zone of an inactive M dwarf. The most detectable feature of organic sulfur gases is an indirect one that results from an increase in ethane (C2H6) over that which would be predicted based on the planet’s methane (CH4) concentration. Thus, a characterization mission could detect these organic sulfur gases—and therefore the life that produces them—if it could sufficiently quantify the ethane and methane in the exoplanet’s atmosphere. Key Words: Exoplanets—Biosignatures—Anoxic atmospheres—Planetary atmospheres—Remote life detection—Photochemistry. Astrobiology 11, 419–441.

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Efficiency of photosynthesis in a Chl d-utilizing cyanobacterium is comparable to or higher than that in Chl a-utilizing oxygenic species (Biochimica Et Biophysica Acta-Bioenergetics, 2011)

The cyanobacterium Acaryochloris marina uses chlorophyll d to carry out oxygenic photosynthesis in environments depleted in visible and enhanced in lower-energy, far-red light. However, the extent to which low photon energies limit the efficiency of oxygenic photochemistry in A. marina is not known. Here, we report the first direct measurements of the energy-storage efficiency of the photosynthetic light reactions in A. marina whole cells, and find it is comparable to or higher than that in typical, chlorophyll a-utilizing oxygenic species. This finding indicates that oxygenic photosynthesis is not fundamentally limited at the photon energies employed by A. marina, and therefore is potentially viable in even longer-wavelength light environments.

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