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DOE OSTI2023

Pumping Iron: A Multi-omics Analysis of Two Extremophilic Algae Reveals Iron Economy Management

Marine algae are responsible for half of the world's primary productivity, but this critical carbonsink is often constrained by insufficient iron. One species of marine algae, Dunaliella tertiolecta, isremarkable for its ability to maintain photosynthesis and thrive in low-iron environments. A relatedspecies, Dunaliella salina Bardawil, shares this attribute but is an extremophile found in hypersaline environments. To elucidate how algae manage their iron requirements, we produced highquality genome assemblies and transcriptomes for both species to serve as a foundation for acomparative multi-omics analysis. We identified a host of iron-uptake proteins in both species,including a massive expansion of transferrins and a novel family of siderophore-iron uptakeproteins. Complementing these multiple iron-uptake routes, ferredoxin functions as a large ironreservoir that can be released by induction of flavodoxin. Proteomic analysis revealed reducedinvestment in the photosynthetic apparatus coupled with remodeling of antenna proteins bydramatic iron-deficiency induction of TIDI1, a light harvesting complex protein found also in otherchlorophytes. These combinatorial iron scavenging and sparing strategies make Dunaliellaunique among photosynthetic organisms

iron homeostasis, phytoplankton, Iron starvation i↗

NASA NTRS2010

Psychrophilic and Psychrotolerant Microbial Extremophiles in Polar Environments

The microbial extremophiles that inhabit the polar regions of our planet are of tremendous significance. The psychrophilic and psychrotolerant microorganisms, which inhabit all of the cold environments on Earth have important applications to Bioremediation, Medicine, Pharmaceuticals, and many other areas of Biotechnology. Until recently, most of the research on polar microorganisms was confined to studies of polar diatoms, yeast, fungi and cyanobacteria. However, within the past three decades, extensive studies have been conducted to understand the bacteria and archaea that inhabit the Arctic and Antarctic sea-ice, glaciers, ice sheets, permafrost and the cryptoendolithic, cryoconite and ice-bubble environments. These investigations have resulted in the discovery of many new genera and species of anaerobic and aerobic microbial extremophiles. Exotic enzymes, cold-shock proteins and pigments produced by some of the extremophiles from polar environments have the potential to be of great benefit to Mankind. Knowledge about microbial life in the polar regions is crucial to understanding the limitations and biodiversity of life on Earth and may provide valuable clues to the Origin of Life on Earth. The discovery of viable microorganisms in ancient ice from the Fox Tunnel, Alaska and the deep Vostok Ice has shown that microorganisms can remain alive while cryopreserved in ancient ice. The psychrophilic lithoautotrophic homoacetogen isolated from the deep anoxic trough of Lake Untersee is an ideal candidate for life that might inhabit comets or the polar caps of Mars. The spontaneous release of gas from within the Anuchin Glacier above Lake Untersee may provide clues to the ice geysers that erupt from the tiger stripe regions of Saturn s moon Enceladus. The methane productivity in the lower regimes of Lake Untersee may also provide insights into possible mechanisms for the recently discovered methane releases on Mars. Since most of the other water bearing bodies of our Solar system are frozen worlds, microbial extremophiles from the Polar Regions of Earth are of great importance to Astrobiology in understanding where and how to search for evidence of life elsewhere in the Cosmos.

Hoover, Richard B.↗

NASA NTRS2010

Development of an Autofluorescence Spectral Database for the Identification and Classification of Microbial Extremophiles

Extremophiles are microorganisms that have adapted to severe conditions that were once considered devoid of life. The extreme settings in which these organisms flourish on earth resemble many extraterrestrial environments. Identification and classification of extremophiles in situ (without the requirement for excessive handling and processing) can provide a basis for designing remotely operated instruments for extraterrestrial life exploration. An important consideration when designing such experiments is to prevent contamination of the environments. We are developing a reference spectral database of autofluorescence from microbial extremophiles using long-UV excitation (405 nm). Aromatic compounds are essential components of living systems, and biological molecules such as aromatic amino acids, nucleotides, porphyrins and vitamins can also exhibit fluorescence under long-UV excitation conditions. Autofluorescence spectra were obtained from a confocal microscope that additionally allowed observations of microbial geometry and motility. It was observed that all extremophiles studied displayed an autofluorescence peak at around 470 nm, followed by a long decay that was species specific. The autofluorescence database can potentially be used as a reference to identify and classify past or present microbial life in our solar system.

Sabanayagam, Chandran↗

DOE OSTI2024

Engineering the Novel Extremophile Alga Chlamydomonas pacifica for High Lipid and High Starch Production as a Path to Developing Commercially Relevant Strains

Microalgae offer a compelling platform for the production of commodity products, due to their superior photosynthetic efficiency, adaptability to nonarable lands and nonpotable water, and their capacity to produce a versatile array of bioproducts, including biofuels and biomaterials. However, the scalability of microalgae as a bioresource has been hindered by challenges such as costly biomass production related to vulnerability to pond crashes during large-scale cultivation. This study presents a pipeline for the genetic engineering and pilot-scale production of biodiesel and thermoplastic polyurethane precursors in the extremophile species Chlamydomonas pacifica. This extremophile microalga exhibits exceptional resilience to high pH (>11.5), high salinity (up to 2% NaCl), and elevated temperatures (up to 42 °C). Initially, we evolved this strain to also have a high tolerance to high light intensity (>2000 μE/m 2 /s) through mutagenesis, breeding, and selection. We subsequently genetically engineered C. pacifica to significantly enhance lipid production by 28% and starch accumulation by 27%, all without affecting its growth rate. We demonstrated the scalability of these engineered strains by cultivating them in pilot-scale raceway ponds and converting the resulting biomass into biodiesel and thermoplastic polyurethanes. This study showcases the complete cycle of transforming a newly discovered species into a commercially relevant commodity production strain. This research underscores the potential of extremophile algae, including C. pacifica, as a key species for the burgeoning sustainable bioeconomy, offering a viable path forward in mitigating environmental challenges and supporting global bioproduct demands.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2007

Microbial Extremophiles in Evolutionary Aspect

Pikuta, Elena V.↗

NASA NTRS2011

Extremophile Diatoms: Implications to the Drake Equation

Diatoms are unicellular Eukaryotes that (as a group and phylogenetically) are not strictly regarded as extremophiles , since the vast majority of diatoms are mesophilic photoautotrophs. However, among the terrestrial Eukaryotes, diatoms are by far the single group of organisms with the ability to inhabit the greatest range of hostile environments on Earth. They are the dominant eukaryotes in the polar regions; in fumaroles, hot springs and geysers; and in hypersaline and hyperalkaline lakes and pools. Cryophilic species such as Fragilaria sublinearis and Chaetoceras fragilis are able to carry out respiration at extremely low rates at low temperatures in darkness. The Drake Equation refers to the likelihood of there being intelligent life at the technological level of electromagnetic communication. However, consideration of the range of conditions suitable for the habitability of eukaryotic diatoms and prokaryotic extremophiles, the likelihood that life exists elsewhere in the cosmos becomes many orders of magnitude greater than that predicted by the classical Drake Equation. In this paper we review the characteristics of diatoms as eukaryotic extremophiles and consider the implications to adjustments needed to the Drake Equation to assess the possibility that life exists elsewhere in the Universe.

Sterrenburg, Frithjof A. S.↗

DOE OSTI2024

Temperature-dependent iron motion in extremophile rubredoxins – no need for ‘corresponding states’

Extremophile organisms are known that can metabolize at temperatures down to – 25 °C (psychrophiles) and up to 122 °C (hyperthermophiles). Understanding viability under extreme conditions is relevant for human health, biotechnological applications, and our search for life elsewhere in the universe. Information about the stability and dynamics of proteins under environmental extremes is an important factor in this regard. Here we compare the dynamics of small Fe-S proteins – rubredoxins – from psychrophilic and hyperthermophilic microorganisms, using three different nuclear techniques as well as molecular dynamics calculations to quantify motion at the Fe site. The theory of ‘corresponding states’ posits that homologous proteins from different extremophiles have comparable flexibilities at the optimum growth temperatures of their respective organisms. Although ‘corresponding states’ would predict greater flexibility for rubredoxins that operate at low temperatures, we find that from 4 to 300 K, the dynamics of the Fe sites in these homologous proteins are essentially equivalent.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Microbial ecology of acidic, biogenic gypsum: community structure and distribution of extremophiles on freshly formed and relict sulfate deposits in a hydrogen sulfide-rich cave

Sulfate minerals are abundant on the Martian surface, and many of these evaporite deposits are thought to have precipitated from acidic fluids. On Earth, gypsum (CaSO 4 •2H 2 O) and other sulfates sometimes form under acidic conditions, so exploring the extremophilic life that occurs in these mineral environments can help evaluate the astrobiological potential of acid sulfate depositional settings. Here, we characterized the microbial communities associated with acidic gypsum deposits in a sulfuric acid cave, where sulfate precipitation is driven by sulfide-oxidizing bacteria and archaea. We used 16S rRNA gene sequencing and cell counts to characterize gypsum-associated microorganisms in freshly formed and relict deposits throughout the cave, to test how microbial community composition and abundance would vary with distance from the sulfidic water table and with the concentration of H 2 S(g) and other gases in the cave atmosphere. We found that actively forming gypsum in the lower cave levels was colonized by low-diversity communities that have few cells compared to other environments in the cave. The most abundant taxa were Acidithiobacillus, Metallibacterium, Mycobacteria, and three different Thermoplasmatales-group archaea, which occupied distinct niches based on proximity to sulfidic streams and the concentration of gases in the cave air. By contrast, deposits in older cave levels had more diverse communities that were distinct from those associated with freshly formed gypsum and likely represent a community reliant on different energy resources. These findings show that acidic sulfate deposits serve as habitats for extremophilic microorganisms and broaden our knowledge of the life associated with terrestrial sulfates.

58 GEOSCIENCES↗

NASA NTRS2003

Identification and Characterization of Extremophile Microorganisms with Significance to Astrobiology

It is now well recognized that microorganisms thrive in extreme ecological conditions such as geothermal vents, polar region, acid and alkaline lakes, and the cold pressurized depth of the ocean floor of this planet. Morphological, physiological, biochemical and genetic adaptations to extreme environments by these extremophile microorganisms have generated immense interest amongst astrobiologists who increasingly believe in the existence of extraterrestrial life. The evidence collected by NASA's space probe Galileo suggested the presence of liquid water and volcanic activity on Mars and Jupiter's satellite Europa. Volcanic activity provides some of the heat necessary to keep the water on Europa from freezing that could provide important dissolved chemicals needed by living organisms. The possibility of the existence of hypersaline alkaline lakes and evaporites confined within closed volcanic basins and impact craters on Mars, and a layer of liquid water under the ice on Europa provide sufficient 'raison d'etre' to study microorganisms in similar extreme environments on Earth, which could provide us with a model that would help establish the existence of extraterrestrial life on other planetary bodies. The objectives of the summer research project were as follows: (1) application of molecular approaches to help establish new species of extremophile microorganisms isolated from a hypersaline alkaline lake; and (2) identification of a major cold-shock gene (cspA) homolog from a psychrotolerant microorganism, PmagG1.

Bej, Asim K.↗

NASA NTRS2007

Astrobiological Significance of Microbial Extremophiles

The microflora of the cryosphere of planet Earth provides the best analogs for life forms that might be found in the permafrost or polar ice caps of Mars, near the surface of the cometary nuclei, or in the liquid water beneath and the ice crusts of icy moons of Jupiter and Saturn. The importance of study alkaliphilic microorganisms for astrobiology was enhanced by the findings of abundant carbonates and carbonate globules rimmed with possibly biogenic magnetites in association with the putative microfossils in the ALH84001 meteorite. Although the ALH84001 "nanofossils" were to small and simple to be unambiguously recognized as biogenic, they stimulated Astrobiology research and studies of microbial extremophiles and biomarkers in ancient rocks and meteorites. Recent studies of CI and CM carbonaceous meteorites have resulted in the detection of the well-preserved mineralized remains of coccoidal and filamentous microorganisms in cyanobacterial mats. Energy Dispersive X-ray Analysis has shown anomalous biogenic element ratios clearly indicating they are not recent biological contaminants. This paper reviews microbial extremophiles in context of their significance to Astrobiology. The study of halophilic microorganisms was started from work with saline soils and lakes, and one of the record of good growth for Haloferax mediterranei was shown at 30 percent NaC1. Although alkali-tolerant nitrifying bacteria had previously been reported, the first described alkaliphilic microorganism was the bacterium Streptococcus faecalis. Halophilic and alkaliphilic forms are relevant to conditions that might be found in closed impact basins and craters on Mars filled with evaporite deposits. The first obligately acidophilic bacterium described was Acidithiobacillus ferrooxydans (formally Thiobacillus ferrooxidans). Later thermophilic lithotrophic acidophiles were found, and the hyperacidophilic moderately thermophilic species of the genus Picrophilus were found to grow at negative pH. The epoch of study of thermophilic microorganisms starts with the discovery of Thermus aquaticus, and presently the maximum temperature for growth at 113 C was found for Pyrolobus fumarii. The microorganisms capable of growth at high temperatures and in hyperacidic environments on Earth are good analogs for life that might be able to survive in hot acidic droplets in the upper regimes of the atmosphere of Venus. The study of barophiles was made possible by engineering achievements leading to the development of the submersible crafts used to study the Black Smokers of the Deep-sea Hydrothermal vents. The first described radioresistant bacterium Deinococcus radiodurans can survive ionizing irradiation and other DNA-damaging assaults at doses that are lethal to all other organisms. These microbes are models for life that might endure high radiation environments in the ice near the surface of comets or on the icy moons of Jupiter and Saturn and in the seafloor deep beneath icy crusts Europa and Enceladus. This paper presents ESEM and FESEM images showing intact microbes preserved in the deep ice cores extracted from just above Lake Vostok, Antarctica that are considered analogs for life forms that might survive on comets and icy moons.

Pikuta, Elena V.↗

NASA NTRS2019

The Critical Role of Extremophiles in Answering the Great Questions of Astrobiology

Astrobiology focuses on the big questions: Where do we come from? Where are we going? And Are we alone? Extremophiles arguably play a large role in answering all three questions, from understanding the location and trajectory of the evolution of life on Earth, to coping with inhabiting a changing home planet. But perhaps the most important role of extremophiles in astrobiology is to understand the potential for life elsewhere. This includes the search for life resulting of an independent origin, as well as moving Earth life off planet into low earth orbit and beyond.

Rothschild, Lynn J.↗

DOE OSTI2023

The carbon-concentrating mechanism of the extremophilic red microalga Cyanidioschyzon merolae

Abstract Cyanidioschyzon merolae is an extremophilic red microalga which grows in low-pH, high-temperature environments. The basis of C. merolae ’s environmental resilience is not fully characterized, including whether this alga uses a carbon-concentrating mechanism (CCM). To determine if C. merolae uses a CCM, we measured CO 2 uptake parameters using an open-path infra-red gas analyzer and compared them to values expected in the absence of a CCM. These measurements and analysis indicated that C. merolae had the gas-exchange characteristics of a CCM-operating organism: low CO 2 compensation point, high affinity for external CO 2 , and minimized rubisco oxygenation. The biomass δ 13 C of C. merolae was also consistent with a CCM. The apparent presence of a CCM in C. merolae suggests the use of an unusual mechanism for carbon concentration, as C. merolae is thought to lack a pyrenoid and gas-exchange measurements indicated that C. merolae primarily takes up inorganic carbon as carbon dioxide, rather than bicarbonate. We use homology to known CCM components to propose a model of a pH-gradient-based CCM, and we discuss how this CCM can be further investigated.

60 APPLIED LIFE SCIENCES↗

NASA NTRS2017

Microbial Extremophiles for Earth and Beyond: Pushing the Boundaries with Synthetic Biology

All organisms live in a multi-dimensional physical and chemical niche space. Discoveries in the 20th century enormously expanded the range of what was considered "habitable." However, the current diversity of life on Earth begs the question of what terrestrial life - or indeed, another life form - would be capable of. With the needs of both modern laboratory science and the burgeoning field of biotechnology, as well as our deeply held desire to answer the question "are we alone in the universe?, we are exploiting the tools of synthetic biology to probe the question of whether we can create "synthetic extremophiles" or, as our lab has dubbed them, "Hell Cells."

synthetic extremophiles↗

DOE OSTI2024

Diverse fates of ancient horizontal gene transfers in extremophilic red algae

Abstract Horizontal genetic transfer (HGT) is a common phenomenon in eukaryotic genomes. However, the mechanisms by which HGT‐derived genes persist and integrate into other pathways remain unclear. This topic is of significant interest because, over time, the stressors that initially favoured the fixation of HGT may diminish or disappear. Despite this, the foreign genes may continue to exist if they become part of a broader stress response or other pathways. The conventional model suggests that the acquisition of HGT equates to adaptation. However, this model may evolve into more complex interactions between gene products, a concept we refer to as the ‘Integrated HGT Model’ (IHM). To explore this concept further, we studied specialized HGT‐derived genes that encode heavy metal detoxification functions. The recruitment of these genes into other pathways could provide clear examples of IHM. In our study, we exposed two anciently diverged species of polyextremophilic red algae from the Galdieria genus to arsenic and mercury stress in laboratory cultures. We then analysed the transcriptome data using differential and coexpression analysis. Our findings revealed that mercury detoxification follows a ‘one gene‐one function’ model, resulting in an indivisible response. In contrast, the ars H gene in the arsenite response pathway demonstrated a complex pattern of duplication, divergence and potential neofunctionalization, consistent with the IHM. Our research sheds light on the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Genetic Transfer in Action: Uncovering DNA Flow in an Extremophilic Microbial Community

ABSTRACT Horizontal genetic transfer (HGT) is a significant driver of genomic novelty in all domains of life. HGT has been investigated in many studies however, the focus has been on conspicuous protein‐coding DNA transfers that often prove to be adaptive in recipient organisms and are therefore fixed longer‐term in lineages. These results comprise a subclass of HGTs and do not represent exhaustive (coding and non‐coding) DNA transfer and its impact on ecology. Uncovering exhaustive HGT can provide key insights into the connectivity of genomes in communities and how these transfers may occur. In this study, we use the term frequency‐inverse document frequency (TF‐IDF) technique, that has been used successfully to mine DNA transfers within real and simulated high‐quality prokaryote genomes, to search for exhaustive HGTs within an extremophilic microbial community. We establish a pipeline for validating transfers identified using this approach. We find that most DNA transfers are within‐domain and involve non‐coding DNA. A relatively high proportion of the predicted protein‐coding HGTs appear to encode transposase activity, restriction‐modification system components, and biofilm formation functions. Our study demonstrates the utility of the TF‐IDF approach for HGT detection and provides insights into the mechanisms of recent DNA transfer.

Microbiology↗

DOE OSTI2023

Increased activity of core photorespiratory enzymes and CO 2 transfer conductances are associated with higher and more optimal photosynthetic rates under elevated temperatures in the extremophile Rhazya stricta

Increase photorespiration and optimising intrinsic water use efficiency are unique challenges to photosynthetic carbon fixation at elevated temperatures. To determine how plants can adapt to facilitate high rates of photorespiration at elevated temperatures while also maintaining water-use efficiency, we performed in-depth gas exchange and biochemical assays of the C 3 extremophile, Rhazya stricta. These results demonstrate that R. stricta supports higher rates of photorespiration under elevated temperatures and that these higher rates of photorespiration correlate with increased activity of key photorespiratory enzymes; phosphoglycolate phosphatase and catalase. The increased photorespiratory enzyme activities may increase the overall capacity of photorespiration by reducing enzymatic bottlenecks and allowing minimal inhibitor accumulation under high photorespiratory rates. Additionally, we found the CO 2 transfer conductances (stomatal and mesophyll) are re-allocated to increase the water-use efficiency in R. stricta but not necessarily the photosynthetic response to temperature. These results suggest important adaptive strategies in R. stricta that maintain photosynthetic rates under elevated temperatures with optimal water loss. The strategies found in R. stricta may inform breeding and engineering efforts in other C 3 species to improve photosynthetic efficiency at high temperatures.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2000

Extremophiles in astrobiology: per Ardua ad Astra

As we consider the possibilities of finding life on other planets, it behooves us to evaluate what we know about the limits for life on planet Earth. In our continued exploration of Earth, we are finding microbes in a variety of unexpected habitats. In geothermal hot springs, we have discovered organisms thriving at temperatures near the boiling point of water and at pH values down to 0.5; in the deepest parts of the oceans, those that grow optimally at pressures above 1000 bars and die at pressures below 500 bars; and at the poles, those that grow below the freezing point of water and die at temperatures above 10 degrees C. All of these organisms are living proof that the biochemical "machinery" of life can be adapted to conditions that, from our anthropocentric perspective, appear to be extreme. By studying the molecular adaptations of extremophiles, we begin to identify the critical cellular components that expand the envelope for life. As an example, I will discuss what we have learned about the role of the proteins we call "heat shock proteins" in pushing the upper temperature limit of life and how our studies have provided a new perspective on the function of these proteins.

Chaperonin 60/physiology↗

NASA NTRS2007

Microbial Extremophiles in Aspect of Limits of Life

During Earth's evolution accompanied by geophysical and climatic changes a number of ecosystems have been formed. These ecosystems differ by the broad variety of physicochemical and biological factors composing our environment. Traditionally, pH and salinity are considered as geochemical extremes, as opposed to the temperature, pressure and radiation that are referred to as physical extremes (Van den Burg, 2003). Life inhabits all possible places on Earth interacting with the environment and within itself (cross species relations). In nature it is very rare when an ecotope is inhabited by a single species. As a rule, most ecosystems contain the functionally related and evolutionarily adjusted communities (consortia and populations). In contrast to the multicellular structure of eukaryotes (tissues, organs, systems of organs, whole organism), the highest organized form of prokaryotic life in nature is the benthic colonization in biofilms and microbial mats. In these complex structures all microbial cells of different species are distributed in space and time according to their functions and to physicochemical gradients that allow more effective system support, self-protection, and energy distribution. In vitro, of course, the most primitive organized structure for bacterial and archaeal cultures is the colony, the size, shape, color, consistency, and other characteristics of which could carry varies specifics on species or subspecies levels. In table 1 all known types of microbial communities are shown (Pikuta et a]., 2005). In deep underground (lithospheric) and deep-sea ecosystems an additional factor - pressure, and irradiation - could also be included in the list of microbial communities. Currently the beststudied ecosystems are: human body (due to the medical importance), and fresh water and marine ecosystems (due to the reason of an environmental safety). For a long time, extremophiles were terra incognita, since the environments with aggressive parameters (compared to the human body temperature, pH, mineralization, and pressure) were considered a priori as a dead zone.

Pikuta, Elena V.↗