skip to main content


Title: Geologic legacy spanning >90 years explains unique Yellowstone hot spring geochemistry and biodiversity
Summary

Little is known about how the geological history of an environment shapes its physical and chemical properties and how these, in turn, influence the assembly of communities. Evening primrose (EP), a moderately acidic hot spring (pH 5.6, 77.4°C) in Yellowstone National Park (YNP), has undergone dramatic physicochemical change linked to seismic activity. Here, we show that this legacy of geologic change led to the development of an unusual sulphur‐rich, anoxic chemical environment that supports a unique archaeal‐dominated and anaerobic microbial community. Metagenomic sequencing and informatics analyses reveal that >96% of this community is supported by dissimilatory reduction or disproportionation of inorganic sulphur compounds, including a novel, deeply diverging sulphate‐reducing thaumarchaeote. When compared to other YNP metagenomes, the inferred functions of EP populations were like those from sulphur‐rich acidic springs, suggesting that sulphur may overprint the predominant influence of pH on the composition of hydrothermal communities. Together, these observations indicate that the dynamic geological history of EP underpins its unique geochemistry and biodiversity, emphasizing the need to consider the legacy of geologic change when describing processes that shape the assembly of communities.

 
more » « less
Award ID(s):
1820658
NSF-PAR ID:
10455446
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
21
Issue:
11
ISSN:
1462-2912
Page Range / eLocation ID:
p. 4180-4195
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Lake sediment microbial communities vary across ecosystems and are often differentiated across pH. Additionally, these pH‐mediated differences in community composition are often correlated with changes in sediment functioning, such as methane and carbon dioxide production. However, few studies have experimentally tested pH effects on community assembly or considered how microbial community composition influences ecosystem function independent of differences in the environment. We used common garden experiments to test hypotheses about how pH influences microbial community assembly and function in lake sediments. Using inoculum from three acidic lakes and three near‐neutral lakes, we found that both pH environment and inoculum source significantly influenced sediment microbial community assembly. However, inoculum source had a larger effect size for both the sediment methanogen and nonmethanogen communities, indicating important roles of dispersal and drift. Additionally, inoculum source, but not pH environment, significantly influenced sediment methane and carbon dioxide production. This research is one of the first to experimentally test the influence of pH on sediment microbial community composition, and in doing so, we show the community composition significantly influences sediment function independent of pH. Understanding how lake sediment microbial communities are influenced by environment is the first step toward mechanistically linking changes in community composition to ecosystem function, and we provide critical evidence for how changes in microbial community assembly with environmental change will likely alter carbon cycling in lake sediments.

     
    more » « less
  2. This Chapter considers triple oxygen isotope variations and their 4 Gyr temporal evolution in bulk siliciclastic sedimentary rocks and in granites. The d18O and D'17O values provide new insights into weathering in the modern and ancient hydrosphere and coeval crustal petrogenesis. We make use of the known geological events and processes that affect the rock cycle: supercontinent assembly and breakup that influence continent-scale and global climate, the fraction of the exposed crust undergoing weathering, and isotopic values of precipitation. New data from a 5000 m Texas drillhole into the Oligocene Frio Formation demonstrate minimal isotopic shifts from mudrocks to shales during diagenesis, mostly related to expulsion of water from smectite-rich loosely cemented sediment and its conversion to illite-rich shale. Inversion of triple oxygen isotope fractionations return isotopic values and temperatures along the hole depth that are more consistent with weathering conditions in the Oligocene and modern North America (d18O = -7 to -15‰, and T of +15 to +45°C) rather than d18O from 8 to 10‰ diagenetic water in the drill hole at 175-195°C. More precise T and d18Owater are obtained where the chemical index of alteration (CIA) based detrital contribution is subtracted from these sediments. Triple oxygen isotopes from suspended sediments in major world rivers record conditions (T and d18Ow) of their watersheds, and not the composition of bedrock because weathering is water-dominated. In parallel, the Chapter presents new analyses of 100 granites, orthogneisses, migmatites, tonalite-trondhjemite-granodiorite (TTG), and large-volume ignimbrites from around the world that range in age from 4 Ga to modern. Most studied granites are orogenic and anatectic in origin and represent large volume remelting/assimilation of shales and other metasediments; the most crustal and high-d18O of these are thus reflect and record the average composition of evolving continental crust. Granites also develop a significant progressive increase in d18O values from 6-7‰ (4-2.5 Ga) to 10-13‰ (~1.8-1.2 Ga) after which d18O stays constant or even decreases. More importantly, we observe a moderate -0.03‰ step-wise decrease in D'17O between 2.1 and 2.5 Ga, which is about half of the step-wise decrease observed in shales over this time interval. We suggest that granites, as well as shales, record the significant advent and greater volumetric appearance of low-D'17O, high-d18O weathering products (shales) altered by meteoric waters upon rapid emergence of large land masses at ~2.4 Ga, although consider alternative interpretations. These weathering products were incorporated into abundant 2.0-1.8 Ga orogens around the world, where upon remelting, they passed their isotopic signature to the granites. We further observe the dichotomy of high-D'17O Archean shales, and unusually low-D'17O Archean granites. We attribute this to greater contribution from shallow crustal hydrothermal contribution to shales in greenstone belts, while granites in the earliest 3.0-4.0 Ga crust and TTGs require involvement of hydrothermal products with lower-D'17O signatures at moderately high-d18O, which we attribute to secondary silicification of their protoliths before partial melting. The Chapter further discusses evolution of the shale record through geologic history and discusses the step-wise change in d18O and D'17O values at Archean/Proterozoic transition. Denser coverage for shales in the past 1 billion years permits investigation of the rocks and their weathering in the last supercontinent cycle, with observed lighter d18O values, characteristic for the mid-Phanerozoic at the initiation of Gondwana breakup. The continuing increase in d18O values of the shales since 4 Ga is interpreted to reflect accumulation of weathering products via shale accretion to continents, as low-density and buoyant shales tend to not subduct back into the mantle. The rock cycle passes triple oxygen isotopic signatures from precipitation to sedimentary, metasedimentary, and finally to anatectic igneous rocks. Continental crust became progressively heavier in d18O, lighter in D'17O due to incremental accumulation of high-d18O sediments in accretionary wedges. Second-order trends in d18O and D'17O are due to supercontinent cycles and glacial episodes. 
    more » « less
  3. Bernstein, Hans C. (Ed.)
    ABSTRACT Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O 2 conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O 2 , sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale -like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium . Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfur oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria , respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O 2 cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O 2 is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O 2 produced in cyanobacterial mat ecosystems. 
    more » « less
  4. Abstract

    Land-use change is highly dynamic globally and there is great uncertainty about the effects of land-use legacies on contemporary environmental performance. We used a chronosequence of urban grasslands (lawns) that were converted from agricultural and forested lands from 10 to over 130 years prior to determine if land-use legacy influences components of soil biodiversity and composition over time. We used historical aerial imagery to identify sites in Baltimore County, MD (USA) with agricultural versus forest land-use history. Soil samples were taken from these sites as well as from existing well-studied agricultural and forest sites used as historical references by the National Science Foundation Long-Term Ecological Research Baltimore Ecosystem Study program. We found that the microbiomes in lawns of agricultural origin were similar to those in agricultural reference sites, which suggests that the ecological parameters on lawns and reference agricultural systems are similar in how they influence soil microbial community dynamics. In contrast, lawns that were previously forest showed distinct shifts in soil bacterial composition upon recent conversion but reverted back in composition similar to forest soils as the lawns aged over decades. Soil fungal communities shifted after forested land was converted to lawns, but unlike bacterial communities, did not revert in composition over time. Our results show that components of bacterial biodiversity and composition are resistant to change in previously forested lawns despite urbanization processes. Therefore land-use legacy, depending on the prior use, is an important factor to consider when examining urban ecological homogenization.

     
    more » « less
  5. Abstract

    Wisconsin's plant communities are responding to shifting disturbance regimes, habitat fragmentation, aerial nitrogen deposition, exotic species invasions, ungulate herbivory, and successional processes. To better understand how plant functional traits mediate species' responses to changing environmental conditions, we collected a large set of functional trait data for vascular plant species occupying Wisconsin forests and grasslands. We used standard protocols to make 76,213 measurements of 34 quantitative traits. These data provide rich information on genome size, physical leaf traits (length, width, circularity, thickness, dry matter content, specific leaf area, etc.), chemical leaf traits (carbon, nitrogen, phosphorus, potassium, calcium, magnesium, ash), life history traits (vegetative and flower heights, seed mass), and traits affecting plant palatability (leaf fiber, fat, and lignin). These trait values derive from replicate measurements on 12+ individuals of each species from multiple sites and 45+ individuals for a selected subset of species. Measurements typically reflect values for individuals although some chemical traits involved composite samples from several individuals at the same site. We also qualitatively characterized each species by plant family, woodiness, functional group, and Raunkiaer lifeform. These data allow us to characterize trait dimensionality, differentiation, and covariation among temperate plant species (e.g., leaf and stem economic syndromes). We can also characterize species' responses to environmental gradients and drivers of ecological change. With survey and resurvey data available from >400 sites in Wisconsin, we can analyze variation in community trait distributions and diversity over time and space. These data therefore allow us to assess how trait divergence vs. convergence affects community assembly and how traits may be related to half‐century shifts in the distribution and abundance of these species. The data set can be used for non‐commercial purposes. The data set is licensed as follows: CC‐By Attribution 4.0 International. We request users cite both the OSF data set and this Ecology data paper publication.

     
    more » « less