Casey Bryce

Impact shocked rocks as protective habitats on an anoxic early Earth

On Earth, microorganisms living under intense ultraviolet (UV) radiation stress can adopt endolithic lifestyles, growing within cracks and pore spaces in rocks. Intense UV irradiation encountered by microbes leads to death and significant damage to biomolecules, which also severely diminishes the likelihood of detecting signatures of life. Here we show that porous rocks shocked by asteroid or comet impacts provide protection for phototrophs and their biomolecules during 22 months of UV radiation exposure outside the International Space Station. The UV spectrum used approximated the high-UV flux on the surface of planets lacking ozone shields such as the early Earth. These data provide a demonstration that endolithic habitats can provide a refugium from the worst-case UV radiation environments on young planets and an empirical refutation of the idea that early intense UV radiation fluxes would have prevented phototrophs without the ability to form microbial mats or produce UV protective pigments from colonizing the surface of early landmasses.

Rock geochemistry induces stress and starvation responses in the bacterial proteome

Interactions between microorganisms and rocks play an important role in Earth system processes. However, little is known about the molecular capabilities microorganisms require to live in rocky environments. Using a quantitative label-free proteomics approach, we show that a model bacterium (Cupriavidus metallidurans CH34) can use volcanic rock to satisfy some elemental requirements, resulting in increased rates of cell division in both magnesium- and iron-limited media. However, the rocks also introduced multiple new stresses via chemical changes associated with pH, elemental leaching and surface adsorption of nutrients that were reflected in the proteome. For example, the loss of bioavailable phosphorus was observed and resulted in the upregulation of diverse phosphate limitation proteins, which facilitate increase phosphate uptake and scavenging within the cell. Our results revealed that despite the provision of essential elements, rock chemistry drives complex metabolic reorganization within rock-dwelling organisms, requiring tight regulation of cellular processes at the protein level. This study advances our ability to identify key microbial responses that enable life to persist in rock environments.

Cryptic biogeochemical cycles: unravelling hidden redox reactions: Cryptic biogeochemical cycles

The turnover of organic matter in the environment is controlled by a series of (often connected) biogeochemical cycles, mainly involving the transformation of C, N, S, O, Fe and Mn under both oxic and anoxic conditions (Druschel and Kappler, 2015). Typically, in order to quantify the extent and rates of turnover, the geochemical end products or reaction intermediates are quantified over time (e.g. sulfide and sulfate or Mn(II) and Mn(IV)). In many cases, the absence of a certain species is used to exclude the relevance of the respective biogeochemical cycle. Recently, however, more evidence has appeared which shows that very reactive, sometimes short-lived intermediates at low concentrations with poorly understood redox properties can play key roles in biogeochemical cycles. For example, redox-active humics are important in carbon cycling, nitrous oxide in the nitrogen cycle and polysulfides in the sulfur cycle (Hansel et al., 2015). The concentrations of these intermediates represent steady-state concentrations arising from the balance between continuous oxidation and reduction. This leads to so-called ‘cryptic element cycles’ where changes in concentrations of a certain redox species cannot be measured but rapid turnover (connected to other element cycles) means that they are key components of the biogeochemical processes that are occurring. In recent years, for example, the importance of cryptic cycling of sulfur has become increasingly clear. The main driver of the sulfur cycle is microbial sulfate reduction which ultimately produces sulfide (H2S). However, this is not a direct process and a large diversity of reactive sulfur species are formed during the six intermediate oxidation states between sulfate and sulfide which are themselves suitable for microbial redox reactions (Zopfi et al., 2004). These reactive intermediates are often below detection limit in the environment, yet are thought to play very important roles in biogeochemical cycling of both sulfur and associated redox species (Holmkvist et al., 2011). Additionally, sulfide can be rapidly recycled making the detection of sulfate reduction difficult. For example, Canfield et al. (2010) found that diverse communities of sulfur cycling microorganisms were present in oxygen minimum zones off the Chilean coast despite very low sulfate and sulfide concentrations. These sulfur cycling communities were sustained through rapid recycling of the H2S which is also linked to nitrogen cycling in these regions. Although cryptic cycling has been described in detail for sulfur, and other elements to a small extent, almost nothing is known about cryptic iron cycling (Hansel et al., 2015).

Oxidation of Fe(II)–Organic Matter Complexes in the Presence of the Mixotrophic Nitrate-Reducing Fe(II)-Oxidizing Bacterium Acidovorax sp. BoFeN1

Fe(II)-organic matter (Fe(II)-OM) complexes are abundant in the environment and may play a key role for the behavior of Fe and pollutants. Mixotrophic nitrate-reducing Fe(II)-oxidizing bacteria (NRFeOx) reduce nitrate coupled to the oxidation of organic compounds and Fe(II). Fe(II) oxidation may occur enzymatically or abiotically by reaction with nitrite that forms during heterotrophic denitrification. However, it is unknown whether Fe(II)-OM complexes can be oxidized by NRFeOx. We used cell-suspension experiments with the mixotrophic nitrate-reducing Fe(II)-oxidizing bacterium Acidovorax sp. strain BoFeN1 to reveal the role of nonorganically bound Fe(II) (aqueous Fe(II)) and nitrite for the rates and extent of oxidation of Fe(II)-OM complexes (Fe(II)-citrate, Fe(II)-EDTA, Fe(II)-humic acid, and Fe(II)-fulvic acid). We found that Fe(II)-OM complexation inhibited microbial nitrate-reducing Fe(II) oxidation; large colloidal and negatively charged complexes showed lower oxidation rates than aqueous Fe(II). Accumulation of nitrite and fast abiotic oxidation of Fe(II)-OM complexes only happened in the presence of aqueous Fe(II) that probably interacted with (nitrite-reducing) enzymes in the periplasm causing nitrite accumulation in the periplasm and outside of the cells, whereas Fe(II)-OM complexes probably could not enter the periplasm and cause nitrite accumulation. These results suggest that Fe(II) oxidation by mixotrophic nitrate reducers in the environment depends on Fe(II) speciation, and that aqueous Fe(II) potentially plays a critical role in regulating microbial denitrification processes.

Microbial anaerobic Fe(II) oxidation - Ecology, mechanisms and environmental implications: Microbial anaerobic Fe(II) oxidation

Iron is the most abundant redox-active metal in the Earths crust. The one electron transfer between the two most common redox states, Fe(II) and Fe(III), plays a role in a huge range of environmental processes from mineral formation and dissolution to contaminant remediation and global biogeochemical cycling. It has been appreciated for more than a century that microorganisms can harness the energy of this Fe redox transformation for their metabolic benefit. However, this is most widely understood for anaerobic Fe(III)-reducing or aerobic and microaerophilic Fe(II)-oxidizing bacteria. Only in the past few decades have we come to appreciate that bacteria also play a role in the anaerobic oxidation of ferrous iron, Fe(II), and thus can act to form Fe(III) minerals in anoxic settings. Since this discovery, our understanding of the ecology of these organisms, their mechanisms of Fe(II) oxidation and their role in environmental processes has been increasing rapidly. In this article, we bring these new discoveries together to review the current knowledge on these environmentally important bacteria, and reveal knowledge gaps for future research.

The UK Centre for Astrobiology : a virtual astrobiology centre. Accomplishments and lessons learned, 2011-2016

Abstract The UK Centre for Astrobiology (UKCA) was set up in 2011 as a virtual center to contribute to astrobiology research, education, and outreach. After 5 years, we describe this center and its work in each of these areas. Its research has focused on studying life in extreme environments, the limits of life on Earth, and implications for habitability elsewhere. Among its research infrastructure projects, UKCA has assembled an underground astrobiology laboratory that has hosted a deep subsurface planetary analog program, and it has developed new flow-through systems to study extraterrestrial aqueous environments. UKCA has used this research backdrop to develop education programs in astrobiology, including a massive open online course in astrobiology that has attracted over 120,000 students, a teacher training program, and an initiative to take astrobiology into prisons. In this paper, we review these activities and others with a particular focus on providing lessons to others who may consider setting up an astrobiology center, institute, or science facility. We discuss experience in integrating astrobiology research into teaching and education activities. Key Words: Astrobiology—Centre—Education—Subsurface—Analog research. Astrobiology 18, 224–243.

Proteome Response of a Metabolically Flexible Anoxygenic Phototroph to Fe(II) Oxidation

The cycling of iron between redox states leads to the precipitation and dissolution of minerals, which can in turn impact other major biogeochemical cycles, such as those of carbon, nitrogen, phosphorus and sulfur. Anoxygenic phototrophs are one of the few drivers of Fe(II) oxidation in anoxic environments and are thought to contribute significantly to iron cycling in both modern and ancient environments. These organisms thrive at high Fe(II) concentrations, yet the adaptations required to tolerate the stresses associated with this are unclear. Despite the general consensus that high Fe(II) concentrations pose numerous stresses on these organisms, our study of the large-scale proteome response of a model anoxygenic phototroph to Fe(II) oxidation demonstrates that common iron homeostasis strategies are adequate to manage this. The bulk of the proteome response is not driven by adaptations to Fe(II) stress but to adaptations required to utilize an inorganic carbon source. Such a global overview of the adaptation of these organisms to Fe(II) oxidation provides valuable insights into the physiology of these biogeochemically important organisms and suggests that Fe(II) oxidation may not pose as many challenges to anoxygenic phototrophs as previously thought. ABSTRACT The oxidation of Fe(II) by anoxygenic photosynthetic bacteria was likely a key contributor to Earths biosphere prior to the evolution of oxygenic photosynthesis and is still found in a diverse range of modern environments. All known phototrophic Fe(II) oxidizers can utilize a wide range of substrates, thus making them very metabolically flexible. However, the underlying adaptations required to oxidize Fe(II), a potential stressor, are not completely understood. We used a combination of quantitative proteomics and cryogenic transmission electron microscopy (cryo-TEM) to compare cells of Rhodopseudomonas palustris TIE-1 grown photoautotrophically with Fe(II) or H2 and photoheterotrophically with acetate. We observed unique proteome profiles for each condition, with differences primarily driven by carbon source. However, these differences were not related to carbon fixation but to growth and light harvesting processes, such as pigment synthesis. Cryo-TEM showed stunted development of photosynthetic membranes in photoautotrophic cultures. Growth on Fe(II) was characterized by a response typical of iron homeostasis, which included an increased abundance of proteins required for metal efflux (particularly copper) and decreased abundance of iron import proteins, including siderophore receptors, with no evidence of further stressors, such as oxidative damage. This study suggests that the main challenge facing anoxygenic phototrophic Fe(II) oxidizers comes from growth limitations imposed by autotrophy, and, once this challenge is overcome, iron stress can be mitigated using iron management mechanisms common to diverse bacteria (e.g., by control of iron influx and efflux). IMPORTANCE The cycling of iron between redox states leads to the precipitation and dissolution of minerals, which can in turn impact other major biogeochemical cycles, such as those of carbon, nitrogen, phosphorus and sulfur. Anoxygenic phototrophs are one of the few drivers of Fe(II) oxidation in anoxic environments and are thought to contribute significantly to iron cycling in both modern and ancient environments. These organisms thrive at high Fe(II) concentrations, yet the adaptations required to tolerate the stresses associated with this are unclear. Despite the general consensus that high Fe(II) concentrations pose numerous stresses on these organisms, our study of the large-scale proteome response of a model anoxygenic phototroph to Fe(II) oxidation demonstrates that common iron homeostasis strategies are adequate to manage this. The bulk of the proteome response is not driven by adaptations to Fe(II) stress but to adaptations required to utilize an inorganic carbon source. Such a global overview of the adaptation of these organisms to Fe(II) oxidation provides valuable insights into the physiology of these biogeochemically important organisms and suggests that Fe(II) oxidation may not pose as many challenges to anoxygenic phototrophs as previously thought.