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1. The recovery of the deep biosphere at the Chicxulub impact crater

   Coolen, M. (January 2018, American Geophysical Union Fall Meeting)

   The Chicxulub crater, Mexico, is the site of the asteroid impact that led to the end-Cretaceous mass extinction. While impact events are known to be able to cause severe disruption to surface-dwelling organisms, the effects of such catastrophic perturbations on the deep biosphere are not known. Deep ocean drilling into the peak ring of the Chicxulub impact crater (IODP expedition 364) in 2016 allowed us to study the modern deep biosphere within the (a) high-porosity melt-bearing impact breccia/suevite (617-740 mbsf) emplaced within a day or so of the Cenozoic, (b) the overlying low porosity post-impact marine Cenozoic carbonates (504-617mbsf), and the impacted and fractured granitic basement (740-1334 mbsf). The microbial biomass (~10 cells/g wet weight) was highest in the upper suevite, in underlying non-granitic subvolcanic pre-impact basanite, and at the intercalation of suevite and impact melt rock. Pre-impact sterile conditions of the uplifted granitic basement rocks and mineralogical evidence of impact-induced sterilization suggest that the basement rocks have only been amenable to microbial colonization for less than 66 Myr. Enrichments at in situ 50-60 °C show the presence of heterotrophic lifestyles in the suevite and bacterial sulfate reduction extending into the top of the granitic basement. Cultivation-independent 16S diversity profiling revealed the presence of heterotrophic (fermentative) as well as autotrophic C-fixing thermophilic bacteria in the organic-rich (up to 4 wt % total organic carbon; TOC) Cenozoic sediments. The organic-lean suevite (< 0.1% TOC) showed the unique presence of sequences related to thermophilic Synechococcus (cyanobacteria) and S-oxidizing green sulfur bacteria (chlorobi), and Chloroflexi often associated with organic-poor deep-sea sediments. Alphaproteobacteria, predominated in the upper part of the granitic basement (<1000 mbsf), while putative manganeseoxidising Bacilli (Firmicutes) predominated in the melt-rich granitic basement (>1200 mbsf). Our data suggest that the catastrophe that led to the end-Cretaceous mass extinction caused geological disruption and recolonization of microbial life in the deep subsurface biosphere at the Chicxulub impact site. 

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2. The Habitat of the Nascent Chicxulub Crater

   https://doi.org/10.1029/2020AV000208  

   Bralower, T. J.; Cosmidis, J.; Fantle, M. S.; Lowery, C. M.; Passey, B. H.; Gulick, S. P. S.; Morgan, J. V.; Vajda, V.; Whalen, M. T.; Wittmann, A.; et al (November 2020, AGU Advances)

   Abstract An expanded sedimentary section provides an opportunity to elucidate conditions in the nascent Chicxulub crater during the hours to millennia after the Cretaceous‐Paleogene (K‐Pg) boundary impact. The sediments were deposited by tsunami followed by seiche waves as energy in the crater declined, culminating in a thin hemipelagic marlstone unit that contains atmospheric fallout. Seiche deposits are predominantly composed of calcite formed by decarbonation of the target limestone during impact followed by carbonation in the water column. Temperatures recorded by clumped isotopes of these carbonates are in excess of 70°C, with heat likely derived from the central impact melt pool. Yet, despite the turbidity and heat, waters within the nascent crater basin soon became a viable habitat for a remarkably diverse cross section of the food chain. The earliest seiche layers deposited with days or weeks of the impact contain earliest Danian nannoplankton and dinocyst survivors. The hemipelagic marlstone representing the subsequent years to a few millennia contains a nearly monogeneric calcareous dinoflagellate resting cyst assemblage suggesting deteriorating environmental conditions, with one interpretation involving low light levels in the impact aftermath. At the same horizon, microbial fossils indicate a thriving bacterial community and unique phosphatic fossils including appendages of pelagic crustaceans, coprolites and bacteria‐tunneled fish bone, suggesting that this rapid recovery of the base of the food chain may have supported the survival of larger, higher trophic‐level organisms. The extraordinarily diverse fossil assemblage indicates that the crater was a unique habitat in the immediate impact aftermath, possibly as a result of heat and nutrients supplied by hydrothermal activity. 

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3. Evidence for autotrophic growth of purple sulfur bacteria using pyrite as electron and sulfur source

   https://doi.org/10.1128/aem.00863-24  

   Alarcon, Hugo V; Mohl, Jonathon E; Chong, Grace W; Betancourt, Ana; Wang, Yi; Leng, Weinan; White, Jason C; Xu, Jie (July 2024, Applied and Environmental Microbiology)

   Spear, John R (Ed.)

   ABSTRACT Purple sulfur bacteria (PSB) are capable of anoxygenic photosynthesis via oxidizing reduced sulfur compounds and are considered key drivers of the sulfur cycle in a range of anoxic environments. In this study, we show thatAllochromatium vinosum(a PSB species) is capable of autotrophic growth using pyrite as the electron and sulfur source. Comparative growth profile, substrate characterization, and transcriptomic sequencing data provided valuable insight into the molecular mechanisms underlying the bacterial utilization of pyrite and autotrophic growth. Specifically, the pyrite-supported cell cultures (“py”’) demonstrated robust but much slower growth rates and distinct patterns from their sodium sulfide-amended positive controls. Up to ~200-fold upregulation of genes encoding variousc- andb-type cytochromes was observed in “py,” pointing to the high relevance of these molecules in scavenging and relaying electrons from pyrite to cytoplasmic metabolisms. Conversely, extensive downregulation of genes related to LH and RC complex components indicates that the electron source may have direct control over the bacterial cells’ photosynthetic activity. In terms of sulfur metabolism, genes encoding periplasmic or membrane-bound proteins (e.g., FccAB and SoxYZ) were largely upregulated, whereas those encoding cytoplasmic proteins (e.g., Dsr and Apr groups) are extensively suppressed. Other notable differentially expressed genes are related to flagella/fimbriae/pilin(+), metal efflux(+), ferrienterochelin(−), and [NiFe] hydrogenases(+). Characterization of the biologically reacted pyrite indicates the presence of polymeric sulfur. These results have, for the first time, put the interplay of PSB and transition metal sulfide chemistry under the spotlight, with the potential to advance multiple fields, including metal and sulfur biogeochemistry, bacterial extracellular electron transfer, and artificial photosynthesis. IMPORTANCEMicrobial utilization of solid-phase substrates constitutes a critical area of focus in environmental microbiology, offering valuable insights into microbial metabolic processes and adaptability. Recent advancements in this field have profoundly deepened our knowledge of microbial physiology pertinent to these scenarios and spurred innovations in biosynthesis and energy production. Furthermore, research into interactions between microbes and solid-phase substrates has directly linked microbial activities to the surrounding mineralogical environments, thereby enhancing our understanding of the relevant biogeochemical cycles. Our study represents a significant step forward in this field by demonstrating, for the first time, the autotrophic growth of purple sulfur bacteria using insoluble pyrite (FeS2) as both the electron and sulfur source. The presented comparative growth profiles, substrate characterizations, and transcriptomic sequencing data shed light on the relationships between electron donor types, photosynthetic reaction center activities, and potential extracellular electron transfer in these organisms capable of anoxygenic photosynthesis. Furthermore, the findings of our study may provide new insights into early-Earth biogeochemical evolutions, offering valuable constraints for understanding the environmental conditions and microbial processes that shaped our planet’s history. 

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4. Selective Uptake of Pelagic Microbial Community Members by Caribbean Reef Corals

   https://doi.org/10.1128/AEM.03175-20  

   Hoadley, Kenneth D.; Hamilton, Maria; Poirier, Camille L.; Choi, Chang Jae; Yung, Cheuk-Man; Worden, Alexandra Z. (April 2021, Applied and Environmental Microbiology)

   Johnson, Karyn N. (Ed.)

   ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down. 

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5. Diel partitioning in microbial phosphorus acquisition in the Sargasso Sea

   https://doi.org/10.1073/pnas.2410268122  

   Muratore, Daniel; Gilbert, Naomi E; LeCleir, Gary R; Wilhelm, Steven W; Weitz, Joshua S (March 2025, Proceedings of the National Academy of Sciences)

   The daily cycle of photosynthetic primary production at the base of marine food webs is often limited by the availability of scarce nutrients. Microbial competition for these scarce resources can be alleviated insofar as the intensity of nutrient uptake and assimilation activities are distributed heterogeneously across organisms over periodic input cycles. Recent analysis of community transcriptional dynamics in the nitrogen-limited subtropical North Pacific gyre revealed evidence of temporal partitioning of nitrogen uptake and assimilation between eukaryotic phytoplankton, cyanobacteria, and heterotrophic bacteria over day-night cycles. Here, we present results from a Lagrangian metatranscriptomic time series survey in the Sargasso Sea and demonstrate temporally partitioned phosphorus uptake in this phosphorus-limited environment. In the Sargasso, heterotrophic bacteria, eukaryotic phytoplankton, and cyanobacteria express genes for phosphorus assimilation during the morning, day, and dusk, respectively. These results support the generality of temporal niche partitioning as an emergent mechanism that can structure uptake of limiting nutrients and facilitate coexistence of diverse microbes in open ocean ecosystems. 

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