Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils.

Periodic oxygen (O2) limitation in humid terrestrial soils likely influences microbial composition, but whether communities share similar responses in disparate environments remains unclear. To test if specific microbial taxa share consistent responses to anoxia in radically different soils, we incubated a rainforest Oxisol and cropland Mollisol under cyclic, time-varying anoxic/oxic cycles in the laboratory. Both soils are known to experience anoxic periods of days to weeks under field conditions; our incubation treatments consisted of anoxic periods of 0, 2, 4, 8, or 12 d followed by 4 d of oxic conditions, repeated for a total of 384 d. Taxa measured by 16S rRNA gene sequences after 48 d and 384 d of experimental treatments varied strongly with increasing anoxic period duration, and responses to anoxia often differed between soils at multiple taxonomic levels. Only 19% of the 30,356 operational taxonomic units (OTUs) occurred in both soils, and most OTUs did not respond consistently to O2 treatments. However, the OTUs present in both soils were disproportionally abundant, comprising 50% of sequences, and they often had a similar response to anoxic period duration in both soils (p < 0.0001). Overall, 67 OTUs, 36 families, 15 orders, 10 classes, and two phyla had significant and directionally consistent (positive or negative) responses to anoxic period duration in both soils. Prominent OTUs and taxonomic groups increasing with anoxic period duration in both soils included actinomycetes (Micromonosporaceae), numerous Ruminococcaceae, possible metal reducers (Anaeromyxobacter) or oxidizers (Candidatus Koribacter), methanogens (Methanomicrobia), and methanotrophs (Methylocystaceae). OTUs decreasing with anoxic duration in both soils included nitrifiers (Nitrospira) and ubiquitous unidentified Bradyrhizobiaceae and Micromonosporaceae. Even within the same genus, different OTUs occasionally showed strong positive or negative responses to anoxic duration (e.g., Dactylosporangium in the Actinobacteria), highlighting a potential for adaptation or niche partitioning in variable-O2 environments. Overall, brief anoxic periods impacted the abundance of certain microbial taxa in predictable ways, suggesting that microbial community data may partially reflect and integrate spatiotemporal differences in O2 availability within and among soils.

Microbial chemolithotrophic oxidation of pyrite in a subsurface shale weathering environment: Geologic considerations and potential mechanisms.

Oxidative weathering of pyrite plays an important role in the biogeochemical cycling of Fe and S in terrestrial environments. While the mechanism and occurrence of biologically accelerated pyrite oxidation under acidic conditions are well established, much less is known about microbially mediated pyrite oxidation at circumneutral pH. Recent work (Percak-Dennett et al., 2017, Geobiology, 15, 690) has demonstrated the ability of aerobic chemolithotrophic microorganisms to accelerate pyrite oxidation at circumneutral pH and proposed two mechanistic models by which this phenomenon might occur. Here, we assess the potential relevance of aerobic microbially catalyzed circumneutral pH pyrite oxidation in relation to subsurface shale weathering at Susquehanna Shale Hills Critical Zone Observatory (SSHCZO) in Pennsylvania, USA. Specimen pyrite mixed with native shale was incubated in groundwater for 3 months at the inferred depth of in situ pyrite oxidation. The colonized materials were used as an inoculum for pyrite-oxidizing enrichment cultures. Microbial activity accelerated the release of sulfate across all conditions. 16S rRNA gene sequencing and metagenomic analysis revealed the dominance of a putative chemolithoautotrophic sulfur-oxidizing bacterium from the genus Thiobacillus in the enrichment cultures. Previously proposed models for aerobic microbial pyrite oxidation were assessed in terms of physical constraints, enrichment culture geochemistry, and metagenomic analysis. Although we conclude that subsurface pyrite oxidation at SSCHZO is largely abiotic, this work nonetheless yields new insight into the potential pathways by which aerobic microorganisms may accelerate pyrite oxidation at circumneutral pH. We propose a new "direct sulfur oxidation" pathway, whereby sulfhydryl-bearing outer membrane proteins mediate oxidation of pyrite surfaces through a persulfide intermediate, analogous to previously proposed mechanisms for direct microbial oxidation of elemental sulfur. The action of this and other direct microbial pyrite oxidation pathways have major implications for controls on pyrite weathering rates in circumneutral pH sedimentary environments where pore throat sizes permit widespread access of microorganisms to pyrite surfaces.

The Weathering Microbiome of an Outcropping Granodiorite.

Microorganisms have long been recognized for their capacity to catalyze the weathering of silicate minerals. While the vast majority of studies on microbially mediated silicate weathering focus on organotrophic metabolism linked to nutrient acquisition, it has been recently demonstrated that chemolithotrophic ferrous iron [Fe(II)] oxidizing bacteria (FeOB) are capable of coupling the oxidation of silicate mineral Fe(II) to metabolic energy generation and cellular growth. In natural systems, complex microbial consortia with diverse metabolic capabilities can exist and interact to influence the biogeochemical cycling of essential elements, including iron. Here we combine microbiological and metagenomic analyses to investigate the potential interactions among metabolically diverse microorganisms in the near surface weathering of an outcrop of the Rio Blanco Quartz Diorite (DIO) in the Luquillo Mountains of Puerto Rico. Laboratory based incubations utilizing ground DIO as metabolic energy source for chemolithotrophic FeOB confirmed the ability of FeOB to grow via the oxidation of silicate-bound Fe(II). Dramatically accelerated rates of Fe(II)-oxidation were associated with an enrichment in microorganisms with the genetic capacity for iron oxidizing extracellular electron transfer (EET) pathways. Microbially oxidized DIO displayed an enhanced susceptibility to the weathering activity of organotrophic microorganisms compared to unoxidized mineral suspensions. Our results suggest that chemolithotrophic and organotrophic microorganisms are likely to coexist and contribute synergistically to the overall weathering of the in situ bedrock outcrop.

Microbially influenced lacustrine carbonates: A comparison of Late Quaternary Lahontan tufa and modern thrombolite from Fayetteville Green Lake, NY.

Carbonate microbialites in lakes can serve as valuable indicators of past environments, so long as the biogenicity and depositional setting of the microbialite can be accurately determined. Late Pleistocene to Early Holocene frondose draping tufa deposits from Winnemucca Dry Lake (Nevada, USA), a subbasin of pluvial Lake Lahontan, were examined in outcrop, petrographically, and geochemically to determine whether microbially induced precipitation is a dominant control on deposition. These observations were compared to modern, actively accumulating microbialites from Fayetteville Green Lake (New York, USA) using similar methods. In addition, preserved microbial DNA was extracted from the Lahontan tufa and sequenced to provide a more complete picture of the microbial communities. Tufas are texturally and geochemically similar to modern thrombolitic microbialites from Fayetteville Green Lake, and the stable isotopic composition of organic C, N, inorganic C, and O supports deposition associated with a lacustrine microbial mat environment dominated by photosynthetic processes. DNA extraction and sequencing indicate that photosynthetic microbial builders were present during tufa deposition, primarily Chloroflexi and Proteobacteria with minor abundances of Cyanobacteria and Acidobacteria. Based on the sequencing results, the depositional environment of the tufas can be constrained to the photic zone of the lake, contrasting with some previous interpretations that put tufa formation in deeper waters. Additionally, the presence of a number of mesothermophilic phyla, including Deinococcus-Thermus, indicates that thermal groundwater may have played a role in tufa deposition at sites not previously associated with groundwater influx. The interpretation of frondose tufas as microbially influenced deposits provides new context to interpretations of lake level and past environments in the Lahontan lake basins.

Microbial chemolithotrophy mediates oxidative weathering of granitic bedrock.

The flux of solutes from the chemical weathering of the continental crust supplies a steady supply of essential nutrients necessary for the maintenance of Earth's biosphere. Promotion of weathering by microorganisms is a well-documented phenomenon and is most often attributed to heterotrophic microbial metabolism for the purposes of nutrient acquisition. Here, we demonstrate the role of chemolithotrophic ferrous iron [Fe(II)]-oxidizing bacteria in biogeochemical weathering of subsurface Fe(II)-silicate minerals at the Luquillo Critical Zone Observatory in Puerto Rico. Under chemolithotrophic growth conditions, mineral-derived Fe(II) in the Rio Blanco Quartz Diorite served as the primary energy source for microbial growth. An enrichment in homologs to gene clusters involved in extracellular electron transfer was associated with dramatically accelerated rates of mineral oxidation and adenosine triphosphate generation relative to sterile diorite suspensions. Transmission electron microscopy and energy-dispersive spectroscopy revealed the accumulation of nanoparticulate Fe-oxyhydroxides on mineral surfaces only under biotic conditions. Microbially oxidized quartz diorite showed greater susceptibility to proton-promoted dissolution, which has important implications for weathering reactions in situ. Collectively, our results suggest that chemolithotrophic Fe(II)-oxidizing bacteria are likely contributors in the transformation of rock to regolith.

Oomycete Species Associated with Soybean Seedlings in North America-Part II: Diversity and Ecology in Relation to Environmental and Edaphic Factors.

Soybean (Glycine max (L.) Merr.) is produced across a vast swath of North America, with the greatest concentration in the Midwest. Root rot diseases and damping-off are a major concern for production, and the primary causal agents include oomycetes and fungi. In this study, we focused on examination of oomycete species distribution in this soybean production system and how environmental and soil (edaphic) factors correlate with oomycete community composition at early plant growth stages. Using a culture-based approach, 3,418 oomycete isolates were collected from 11 major soybean-producing states and most were identified to genus and species using the internal transcribed spacer region of the ribosomal DNA. Pythium was the predominant genus isolated and investigated in this study. An ecology approach was taken to understand the diversity and distribution of oomycete species across geographical locations of soybean production. Metadata associated with field sample locations were collected using geographical information systems. Operational taxonomic units (OTU) were used in this study to investigate diversity by location, with OTU being defined as isolate sequences with 97% identity to one another. The mean number of OTU ranged from 2.5 to 14 per field at the state level. Most OTU in this study, classified as Pythium clades, were present in each field in every state; however, major differences were observed in the relative abundance of each clade, which resulted in clustering of states in close proximity. Because there was similar community composition (presence or absence) but differences in OTU abundance by state, the ordination analysis did not show strong patterns of aggregation. Incorporation of 37 environmental and edaphic factors using vector-fitting and Mantel tests identified 15 factors that correlate with the community composition in this survey. Further investigation using redundancy analysis identified latitude, longitude, precipitation, and temperature as factors that contribute to the variability observed in community composition. Soil parameters such as clay content and electrical conductivity also affected distribution of oomycete species. The present study suggests that oomycete species composition across geographical locations of soybean production is affected by a combination of environmental and edaphic conditions. This knowledge provides the basis to understand the ecology and distribution of oomycete species, especially those able to cause diseases in soybean, providing cues to develop management strategies.

Oomycete Species Associated with Soybean Seedlings in North America-Part I: Identification and Pathogenicity Characterization.

Oomycete pathogens are commonly associated with soybean root rot and have been estimated to reduce soybean yields in the United States by 1.5 million tons on an annual basis. Limited information exists regarding the frequency and diversity of oomycete species across the major soybean-producing regions in North America. A survey was conducted across 11 major soybean-producing states in the United States and the province of Ontario, Canada. In 2011, 2,378 oomycete cultures were isolated from soybean seedling roots on a semiselective medium (CMA-PARPB) and were identified by sequencing of the internal transcribed spacer region of rDNA. Sequence results distinguished a total of 51 Pythium spp., three Phytophthora spp., three Phytopythium spp., and one Aphanomyces sp. in 2011, with Pythium sylvaticum (16%) and P. oopapillum (13%) being the most prevalent. In 2012, the survey was repeated, but, due to drought conditions across the sampling area, fewer total isolates (n = 1,038) were collected. Additionally, in 2012, a second semiselective medium (V8-RPBH) was included, which increased the Phytophthora spp. isolated from 0.7 to 7% of the total isolates. In 2012, 54 Pythium spp., seven Phytophthora spp., six Phytopythium spp., and one Pythiogeton sp. were recovered, with P. sylvaticum (14%) and P. heterothallicum (12%) being recovered most frequently. Pathogenicity and virulence were evaluated with representative isolates of each of the 84 species on soybean cv. Sloan. A seed-rot assay identified 13 and 11 pathogenic species, respectively, at 13 and 20°C. A seedling-root assay conducted at 20°C identified 43 species as pathogenic, having a significantly detrimental effect on the seedling roots as compared with the noninoculated control. A total of 15 species were pathogenic in both the seed and seedling assays. This study provides a comprehensive characterization of oomycete species present in soybean seedling roots in the major production areas in the United States and Ontario, Canada and provides a basis for disease management and breeding programs.