Antimicrobial Activity of Metals and Metalloids.

Competition shapes evolution. Toxic metals and metalloids have exerted selective pressure on life since the rise of the first organisms on the Earth, which has led to the evolution and acquisition of resistance mechanisms against them, as well as mechanisms to weaponize them. Microorganisms exploit antimicrobial metals and metalloids to gain competitive advantage over other members of microbial communities. This exerts a strong selective pressure that drives evolution of resistance. This review describes, with a focus on arsenic and copper, how microorganisms exploit metals and metalloids for predation and how metal- and metalloid-dependent predation may have been a driving force for evolution of microbial resistance against metals and metalloids.

Organism motility in an oxygenated shallow-marine environment 2.1 billion years ago.

Evidence for macroscopic life in the Paleoproterozoic Era comes from 1.8 billion-year-old (Ga) compression fossils [Han TM, Runnegar B (1992) Science 257:232-235; Knoll et al. (2006) Philos Trans R Soc Lond B 361:1023-1038], Stirling biota [Bengtson S et al. (2007) Paleobiology 33:351-381], and large colonial organisms exhibiting signs of coordinated growth from the 2.1-Ga Francevillian series, Gabon. Here we report on pyritized string-shaped structures from the Francevillian Basin. Combined microscopic, microtomographic, geochemical, and sedimentologic analyses provide evidence for biogenicity, and syngenicity and suggest that the structures underwent fossilization during early diagenesis close to the sediment-water interface. The string-shaped structures are up to 6 mm across and extend up to 170 mm through the strata. Morphological and 3D tomographic reconstructions suggest that the producer may have been a multicellular or syncytial organism able to migrate laterally and vertically to reach food resources. A possible modern analog is the aggregation of amoeboid cells into a migratory slug phase in cellular slime molds at times of starvation. This unique ecologic window established in an oxygenated, shallow-marine environment represents an exceptional record of the biosphere following the crucial changes that occurred in the atmosphere and ocean in the aftermath of the great oxidation event (GOE).

Cu isotopes in marine black shales record the Great Oxidation Event.

The oxygenation of the atmosphere ∼2.45-2.32 billion years ago (Ga) is one of the most significant geological events to have affected Earth's redox history. Our understanding of the timing and processes surrounding this key transition is largely dependent on the development of redox-sensitive proxies, many of which remain unexplored. Here we report a shift from negative to positive copper isotopic compositions (δ(65)CuERM-AE633) in organic carbon-rich shales spanning the period 2.66-2.08 Ga. We suggest that, before 2.3 Ga, a muted oxidative supply of weathering-derived copper enriched in (65)Cu, along with the preferential removal of (65)Cu by iron oxides, left seawater and marine biomass depleted in (65)Cu but enriched in (63)Cu. As banded iron formation deposition waned and continentally sourced Cu became more important, biomass sampled a dissolved Cu reservoir that was progressively less fractionated relative to the continental pool. This evolution toward heavy δ(65)Cu values coincides with a shift to negative sedimentary δ(56)Fe values and increased marine sulfate after the Great Oxidation Event (GOE), and is traceable through Phanerozoic shales to modern marine settings, where marine dissolved and sedimentary δ(65)Cu values are universally positive. Our finding of an important shift in sedimentary Cu isotope compositions across the GOE provides new insights into the Precambrian marine cycling of this critical micronutrient, and demonstrates the proxy potential for sedimentary Cu isotope compositions in the study of biogeochemical cycles and oceanic redox balance in the past.

Bioreactor studies predict whole microbial population dynamics in oil sands tailings ponds.

Microorganisms in oil sands fluid fine tailings (FFT) are critical to biogeochemical elemental cycling as well as to the degradation of residual hydrocarbon constituents and subsequent methane and CO2 production. Microbial activity enhances particulate matter sedimentation rates and the dewatering of FFT materials, allowing water to be recycled back into bitumen extraction. A bulk of this evidence comes from bioreactor studies and has implications for engineering and environmental management of the FFT ponds. Yet, it is largely uncertain whether such laboratory populations are representative of whole field scale microbial communities. By using population ecology tools, we compared whole microbial communities present in FFT bioreactors to reference populations existing in Syncrude's West In Pit (WIP) tailings pond. Bacteria were found to be persistent in a sulfidic zone in both the oxic and anoxic bioreactors at all occasions tested. In contrast to the WIP, archaea only became predominant in bioreactors after 300 days, at which point analysis of similarity (global R statistic p<0.5) revealed no significant dissimilarities between the populations present in either system. A whole community succession pattern from bacterial dominated prevalence to a new assemblage predominated by archaea was suggested. These results have implications for the stepwise development of microbial model systems for predictive management of field scale FFT basins.

Blooming of a microbial community in an Ediacaran extreme volcanic lake system.

Ancient aquatic sediments are critical archives for studying early microbial life and the types of environments in which they thrived. The recently characterized Amane Tazgart microbialites in the Anti-Atlas, Morocco, are a rare and well-preserved non-marine deposit that evolved in an alkaline volcanic lake setting during the Ediacaran Period. A multiproxy geochemical toolbox reveals evidence pointing to spatio-temporal ecosystem organization and succession related to changing lake water chemistry. This is marked by secular transition from a cold/dry climate, hypersaline alkaline thermophilic and anoxic-oxic community, to a stable state warm/wet climate fully oxygenated fresh to brackish water ecosystem, predominated by oxygenic stromatolites. Extreme dissolved Arsenic concentrations suggest that these polyextremophiles required robust detoxification mechanisms to circumvent arsenic toxicity and phosphate deficiency. We propose that self-sustaining and versatile anoxic to oxic microbial ecosystems thrived in aquatic continental settings during the Ediacaran Period, when complex life co-evolved with a rise in atmospheric oxygen content.

Non-linear population dynamics in chemostats associated with live-dead cell cycling in Escherichia coli strain K12-MG1655.

Bacterial populations conditionally display non-linear dynamic behaviour in bioreactors with steady inputs, which is often attributed to varying habitat conditions or shifting intracellular metabolic activity. However, mathematical modelling has predicted that such dynamics also might simply result from staggered birth, growth, and death events of groups of cells within the population, causing density oscillations and the cycling of live and dead cells within the system. To assess this prediction, laboratory experiments were performed on Escherichia coli strain K12-MG1655 grown in chemostats to first define fine-scale population dynamics over time (minutes) and then determine whether the dynamics correlate with live-dead cell cycles in the system. E. coli populations displayed consistent oscillatory behaviour in all experiments. However, close synchronisation between OD600 and live-dead cell oscillations (within ~33-38 min cycles) only became statistically significant (p < 0.01) when pseudo-steady state operations approaching carrying capacity existed in the bioreactor. Specifically, live cells were highest at local OD600 maxima and lowest at local OD600 minima, showing that oscillations followed live-dead cell cycles as predicted by the model and also consistent with recent observations that death is non-stochastic in such populations. These data show that oscillatory dynamic behaviour is intrinsic in bioreactor populations, which has implications to process operations in biotechnology.

A 571 million-year-old alkaline volcanic lake photosynthesizing microbial community, the Anti-atlas, Morocco.

The Ediacaran period coincides with the emergence of ancestral animal lineages and cyanobacteria capable of thriving in nutrient deficient oceans which together with photosynthetic eukaryotic dominance, culminated in the rapid oxygenation of the Ediacaran atmosphere. However, ecological evidence for the colonization of the Ediacaran terrestrial biosphere by photosynthetic communities and their contribution to the oxygenation of the biosphere at this time is very sparse. Here, we expand the repertoire of Ediacaran habitable environments to a specific microbial community that thrived in an extreme alkaline volcanic lake 571 Myr ago in the Anti-atlas of Morocco. The microbial fabrics preserve evidence of primary growth structures, comprised of two main microbialitic units, with the lower section consisting of irregular and patchy thrombolytic mesoclots associated with composite microbialitic domes. Calcirudite interbeds, dominated by wave-rippled sandy calcarenites and stromatoclasts, fill the interdome troughs and seal the dome tops. A meter-thick epiclastic stromatolite bed grading upwards from a dominantly flat to wavy laminated base, transitions into low convex laminae consisting of decimeter to meter-thick dome-shaped stromatolitic columns, overlies the thrombolitic and composite microbialitic facies. Microbialitic beds constructed during periods of limited clastic input, and underlain by coarse-grained microbialite-derived clasts and by the wave-rippled calcarenites, suggest high-energy events associated with lake expansion. High-resolution microscopy revealed spherulitic aggregates and structures reminiscent of coccoidal microbial cell casts and mineralized extra-polymeric substances (EPS). The primary fabrics and multistage diagenetic features, represented by active carbonate production, photosynthesizing microbial communities, photosynthetic gas bubbles, gas escape structures, and tufted mats, suggest specialized oxygenic photosynthesizers thriving in alkaline volcanic lakes, contributed toward oxygen variability in the Ediacaran terrestrial biosphere.

Unusual microbial mat-related structural diversity 2.1 billion years ago and implications for the Francevillian biota.

The 2.1-billion-year-old (Ga) Francevillian series in Gabon hosts some of the oldest reported macroscopic fossils of various sizes and shapes, stimulating new debates on the origin, evolution and organization of early complex life. Here, we document ten representative types of exceptionally well-preserved mat-related structures, comprising "elephant-skin" textures, putative macro-tufted microbial mats, domal buildups, flat pyritized structures, discoidal microbial colonies, horizontal mat growth patterns, wrinkle structures, "kinneyia" structures, linear patterns and nodule-like structures. A combination of petrographic analyses, scanning electron microscopy, Raman spectroscopy and organic elemental analyses of carbon-rich laminae and microtexture, indicate a biological origin for these structures. The observed microtextures encompass oriented grains, floating silt-sized quartz grains, concentrated heavy minerals, randomly oriented clays, wavy-crinkly laminae and pyritized structures. Based on comparisons with modern analogues, as well as an average δ13 C organic matter (Corg ) composition of -32.94 ± 1.17‰ (1 standard deviation, SD) with an outlier of -41.26‰, we argue that the mat-related structures contain relicts of multiple carbon pathways including heterotrophic recycling of photosynthetically derived Corg . Moreover, the relatively close association of the macroscopic fossil assemblages to the microbial mats may imply that microbial communities acted as potential benthic O2 oases linked to oxyphototrophic cyanobacterial mats and grazing grounds. In addition, the mat's presence likely improved the preservation of the oldest large colonial organisms, as they are known to strongly biostabilize sediments. Our findings highlight the oldest community assemblage of microscopic and macroscopic biota in the aftermath of the "Great Oxidation Event," widening our understanding of biological organization during Earth's middle age.

Methane fluxes from coastal sediments are enhanced by macrofauna.

Methane and nitrous oxide are potent greenhouse gases (GHGs) that contribute to climate change. Coastal sediments are important GHG producers, but the contribution of macrofauna (benthic invertebrates larger than 1 mm) inhabiting them is currently unknown. Through a combination of trace gas, isotope, and molecular analyses, we studied the direct and indirect contribution of two macrofaunal groups, polychaetes and bivalves, to methane and nitrous oxide fluxes from coastal sediments. Our results indicate that macrofauna increases benthic methane efflux by a factor of up to eight, potentially accounting for an estimated 9.5% of total emissions from the Baltic Sea. Polychaetes indirectly enhance methane efflux through bioturbation, while bivalves have a direct effect on methane release. Bivalves host archaeal methanogenic symbionts carrying out preferentially hydrogenotrophic methanogenesis, as suggested by analysis of methane isotopes. Low temperatures (8 °C) also stimulate production of nitrous oxide, which is consumed by benthic denitrifying bacteria before it reaches the water column. We show that macrofauna contributes to GHG production and that the extent is dependent on lineage. Thus, macrofauna may play an important, but overlooked role in regulating GHG production and exchange in coastal sediment ecosystems.

The 2.1 Ga old Francevillian biota: biogenicity, taphonomy and biodiversity.

The Paleoproterozoic Era witnessed crucial steps in the evolution of Earth's surface environments following the first appreciable rise of free atmospheric oxygen concentrations ∼2.3 to 2.1 Ga ago, and concomitant shallow ocean oxygenation. While most sedimentary successions deposited during this time interval have experienced thermal overprinting from burial diagenesis and metamorphism, the ca. 2.1 Ga black shales of the Francevillian B Formation (FB2) cropping out in southeastern Gabon have not. The Francevillian Formation contains centimeter-sized structures interpreted as organized and spatially discrete populations of colonial organisms living in an oxygenated marine ecosystem. Here, new material from the FB2 black shales is presented and analyzed to further explore its biogenicity and taphonomy. Our extended record comprises variably sized, shaped, and structured pyritized macrofossils of lobate, elongated, and rod-shaped morphologies as well as abundant non-pyritized disk-shaped macrofossils and organic-walled acritarchs. Combined microtomography, geochemistry, and sedimentary analysis suggest a biota fossilized during early diagenesis. The emergence of this biota follows a rise in atmospheric oxygen, which is consistent with the idea that surface oxygenation allowed the evolution and ecological expansion of complex megascopic life.

Fossilized iron bacteria reveal a pathway to the biological origin of banded iron formation.

Debates on the formation of banded iron formations in ancient ferruginous oceans are dominated by a dichotomy between abiotic and biotic iron cycling. This is fuelled by difficulties in unravelling the exact processes involved in their formation. Here we provide fossil environmental evidence for anoxygenic photoferrotrophic deposition of analogue banded iron rocks in shallow marine waters associated with an Early Quaternary hydrothermal vent field on Milos Island, Greece. Trace metal, major and rare earth elemental compositions suggest that the deposited rocks closely resemble banded iron formations of Precambrian origin. Well-preserved microbial fossils in combination with chemical data imply that band formation was linked to periodic massive encrustation of anoxygenic phototrophic biofilms by iron oxyhydroxide alternating with abiotic silica precipitation. The data implicate cyclic anoxygenic photoferrotrophy and their fossilization mechanisms in the construction of microskeletal fabrics that result in the formation of characteristic banded iron formation bands of varying silica and iron oxide ratios.