Cardon Zoe G.

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Cardon

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Zoe G.

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Extraction of high-quality, high-molecular-weight DNA depends heavily on cell homogenization methods in green microalgae

(Wiley Open Access, 2020-03-10) Stark, Jordan R. ; Cardon, Zoe G. ; Peredo, Elena L.

Premise New sequencing technologies have facilitated genomic studies in green microalgae; however, extracting high‐quality DNA is often a bottleneck for long‐read sequencing. Methods and Results Here, we present a low‐cost, highly transferrable method for the extraction of high‐molecular‐weight (HMW), high‐purity DNA from microalgae. We first determined the effect of sample preparation on DNA quality using three homogenization methods: manual grinding using a mini‐pestle, automatic grinding using a vortex adapter, and grinding in liquid nitrogen. We demonstrated the versatility of grinding in liquid nitrogen followed by a modified cetyltrimethylammonium bromide (CTAB) extraction across a suite of aquatic‐ and desert‐evolved algal taxa. Finally, we tested the protocol's robustness by doubling the input material to increase yield, producing per sample up to 20 μg of high‐purity DNA longer than 21.2 kbp. Conclusions All homogenization methods produced DNA within acceptable parameters for purity, but only liquid nitrogen grinding resulted in HMW DNA. The optimization of cell lysis while minimizing DNA shearing is therefore crucial for the isolation of DNA for long‐read genomic sequencing because template DNA length strongly affects read output and length.
Better to light a candle than curse the darkness : illuminating spatial localization and temporal dynamics of rapid microbial growth in the rhizosphere

(Frontiers Media, 2013-09-02) Herron, Patrick M. ; Gage, Daniel J. ; Pinedo, Catalina Arango ; Haider, Zane K. ; Cardon, Zoe G.

The rhizosphere is a hotbed of microbial activity in ecosystems, fueled by carbon compounds from plant roots. Basic questions about the location and dynamics of plant-spurred microbial growth in the rhizosphere are difficult to answer with standard, destructive soil assays mixing a multitude of microbe-scale microenvironments in a single, often sieved, sample. Soil microbial biosensors designed with the luxCDABE reporter genes fused to a promoter of interest enable continuous imaging of the microbial perception of (and response to) environmental conditions in soil. We used the common soil bacterium Pseudomonas putida KT2440 as host to plasmid pZKH2 containing a fusion between the strong constitutive promoter nptII and luxCDABE (coding for light-emitting proteins) from Vibrio fischeri. Experiments in liquid media demonstrated that high light production by KT2440/pZKH2 was associated with rapid microbial growth supported by high carbon availability. We applied the biosensors in microcosms filled with non-sterile soil in which corn (Zea mays L.), black poplar (Populus nigra L.), or tomato (Solanum lycopersicum L.) was growing. We detected minimal light production from microbiosensors in the bulk soil, but biosensors reported continuously from around roots for as long as six days. For corn, peaks of luminescence were detected 1–4 and 20–35 mm along the root axis behind growing root tips, with the location of maximum light production moving farther back from the tip as root growth rate increased. For poplar, luminescence around mature roots increased and decreased on a coordinated diel rhythm, but was not bright near root tips. For tomato, luminescence was dynamic, but did not exhibit a diel rhythm, appearing in acropetal waves along roots. KT2440/pZKH2 revealed that root tips are not always the only, or even the dominant, hotspots for rhizosphere microbial growth, and carbon availability is highly variable in space and time around roots. - See more at: http://journal.frontiersin.org/Journal/10.3389/fpls.2013.00323/full#sthash.Bv7U0hD6.dpuf
The green algal underground : evolutionary secrets of desert cells

(American Institute of Biological Sciences, 2008-02) Cardon, Zoe G. ; Gray, Dennis W. ; Lewis, Louise A.

Microscopic, unicellular, free-living green algae are found in desert microbiotic crusts worldwide. Although morphologically simple, green algae in desert crusts have recently been found to be extraordinarily diverse, with membership spanning five green algal classes and encompassing many taxa new to science. This overview explores this remarkable diversity and its potential to lead to new perspectives on the diversity and evolution of green plants. Molecular systematic and physiological data gathered from desert taxa demonstrate that these algae are long-term members of desert communities, not transient visitors from aquatic habitats. Variations in desiccation tolerance and photophysiology among these algae include diverse evolutionary innovations that developed under selective pressures in the desert. Combined with the single embryophyte lineage to which more familiar terrestrial green plants belong, multiple desert green algal lineages provide independent evolutionary units that may enhance understanding of the evolution and ecology of eukaryotic photosynthetic life on land.
Combined measurement and modeling of the hydrological impact of hydraulic redistribution using CLM4.5 at eight AmeriFlux sites

(Copernicus Publications on behalf of the European Geosciences Union, 2016-05-17) Fu, Congsheng ; Wang, Guiling ; Goulden, Michael L. ; Scott, Russell L. ; Bible, Kenneth ; Cardon, Zoe G.

Effects of hydraulic redistribution (HR) on hydrological, biogeochemical, and ecological processes have been demonstrated in the field, but the current generation of standard earth system models does not include a representation of HR. Though recent studies have examined the effect of incorporating HR into land surface models, few (if any) have done cross-site comparisons for contrasting climate regimes and multiple vegetation types via the integration of measurement and modeling. Here, we incorporated the HR scheme of Ryel et al. (2002) into the NCAR Community Land Model Version 4.5 (CLM4.5), and examined the ability of the resulting hybrid model to capture the magnitude of HR flux and/or soil moisture dynamics from which HR can be directly inferred, to assess the impact of HR on land surface water and energy budgets, and to explore how the impact may depend on climate regimes and vegetation conditions. Eight AmeriFlux sites with contrasting climate regimes and multiple vegetation types were studied, including the Wind River Crane site in Washington State, the Santa Rita Mesquite savanna site in southern Arizona, and six sites along the Southern California Climate Gradient. HR flux, evapotranspiration (ET), and soil moisture were properly simulated in the present study, even in the face of various uncertainties. Our cross-ecosystem comparison showed that the timing, magnitude, and direction (upward or downward) of HR vary across ecosystems, and incorporation of HR into CLM4.5 improved the model-measurement matches of evapotranspiration, Bowen ratio, and soil moisture particularly during dry seasons. Our results also reveal that HR has important hydrological impact in ecosystems that have a pronounced dry season but are not overall so dry that sparse vegetation and very low soil moisture limit HR.
Tools for the microbiome : nano and beyond

(American Chemical Society, 2015-12-22) Biteen, Julie S. ; Blainey, Paul C. ; Cardon, Zoe G. ; Chun, Miyoung ; Church, George M. ; Dorrestein, Pieter C. ; Fraser, Scott E. ; Gilbert, Jack A. ; Jansson, Janet K. ; Knight, Rob ; Miller, Jeff F. ; Ozcan, Aydogan ; Prather, Kimberly A. ; Quake, Stephen R. ; Ruby, Edward G. ; Silver, Pamela A. ; Taha, Sharif ; van den Engh, Ger ; Weiss, Paul S. ; Wong, Gerard C. L. ; Wright, Aaron T. ; Young, Thomas D.

The microbiome presents great opportunities for understanding and improving the world around us and elucidating the interactions that compose it. The microbiome also poses tremendous challenges for mapping and manipulating the entangled networks of interactions among myriad diverse organisms. Here, we describe the opportunities, technical needs, and potential approaches to address these challenges, based on recent and upcoming advances in measurement and control at the nanoscale and beyond. These technical needs will provide the basis for advancing the largely descriptive studies of the microbiome to the theoretical and mechanistic understandings that will underpin the discipline of microbiome engineering. We anticipate that the new tools and methods developed will also be more broadly useful in environmental monitoring, medicine, forensics, and other areas.
Extended local similarity analysis (eLSA) of microbial community and other time series data with replicates

(BioMed Central, 2011-12-14) Xia, Li C. ; Steele, Joshua A. ; Cram, Jacob A. ; Cardon, Zoe G. ; Simmons, Sheri L. ; Vallino, Joseph J. ; Fuhrman, Jed A. ; Sun, Fengzhu

The increasing availability of time series microbial community data from metagenomics and other molecular biological studies has enabled the analysis of large-scale microbial co-occurrence and association networks. Among the many analytical techniques available, the Local Similarity Analysis (LSA) method is unique in that it captures local and potentially time-delayed co-occurrence and association patterns in time series data that cannot otherwise be identified by ordinary correlation analysis. However LSA, as originally developed, does not consider time series data with replicates, which hinders the full exploitation of available information. With replicates, it is possible to understand the variability of local similarity (LS) score and to obtain its confidence interval. We extended our LSA technique to time series data with replicates and termed it extended LSA, or eLSA. Simulations showed the capability of eLSA to capture subinterval and time-delayed associations. We implemented the eLSA technique into an easy-to-use analytic software package. The software pipeline integrates data normalization, statistical correlation calculation, statistical significance evaluation, and association network construction steps. We applied the eLSA technique to microbial community and gene expression datasets, where unique time-dependent associations were identified. The extended LSA analysis technique was demonstrated to reveal statistically significant local and potentially time-delayed association patterns in replicated time series data beyond that of ordinary correlation analysis. These statistically significant associations can provide insights to the real dynamics of biological systems. The newly designed eLSA software efficiently streamlines the analysis and is freely available from the eLSA homepage, which can be accessed at http://meta.usc.edu/softs/lsa
A model suite of green algae within the Scenedesmaceae for investigating contrasting desiccation tolerance and morphology

(The Company of Biologists, 2018-04-10) Cardon, Zoe G. ; Peredo, Elena L. ; Dohnalkova, Alice C. ; Gershone, Hannah L. ; Bezanilla, Magdalena

Microscopic green algae inhabiting desert microbiotic crusts are remarkably diverse phylogenetically, and many desert lineages have independently evolved from aquatic ancestors. Here we worked with five desert and aquatic species within the family Scenedesmaceae to examine mechanisms that underlie desiccation tolerance and release of unicellular versus multicellular progeny. Live cell staining and time-lapse confocal imaging coupled with transmission electron microscopy established that the desert and aquatic species all divide by multiple (rather than binary) fission, although progeny were unicellular in three species and multicellular (joined in a sheet-like coenobium) in two. During division, Golgi complexes were localized near nuclei, and all species exhibited dynamic rotation of the daughter cell mass within the mother cell wall at cytokinesis. Differential desiccation tolerance across the five species, assessed from photosynthetic efficiency during desiccation/rehydration cycles, was accompanied by differential accumulation of intracellular reactive oxygen species (ROS) detected using a dye sensitive to intracellular ROS. Further comparative investigation will aim to understand the genetic, ultrastructural and physiological characteristics supporting unicellular versus multicellular coenobial morphology, and the ability of representatives in the Scenedesmaceae to colonize ecologically diverse, even extreme, habitats.
Toward a predictive understanding of Earth’s microbiomes to address 21st century challenges

(American Society for Microbiology, 2016-05-13) Blaser, Martin J. ; Cardon, Zoe G. ; Cho, Mildred K. ; Dangl, Jeffery ; Donohue, Timothy J. ; Green, Jessica L. ; Knight, Rob ; Maxon, Mary E. ; Northen, Trent R. ; Pollard, Katherine ; Brodie, Eoin L.

Microorganisms have shaped our planet and its inhabitants for over 3.5 billion years. Humankind has had a profound influence on the biosphere, manifested as global climate and land use changes, and extensive urbanization in response to a growing population. The challenges we face to supply food, energy, and clean water while maintaining and improving the health of our population and ecosystems are significant. Given the extensive influence of microorganisms across our biosphere, we propose that a coordinated, cross-disciplinary effort is required to understand, predict, and harness microbiome function. From the parallelization of gene function testing to precision manipulation of genes, communities, and model ecosystems and development of novel analytical and simulation approaches, we outline strategies to move microbiome research into an era of causality. These efforts will improve prediction of ecosystem response and enable the development of new, responsible, microbiome-based solutions to significant challenges of our time.
Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae

(National Academy of Sciences, 2020-07-21) Peredo, Elena L. ; Cardon, Zoe G.

Among green plants, desiccation tolerance is common in seeds and spores but rare in leaves and other vegetative green tissues. Over the last two decades, genes have been identified whose expression is induced by desiccation in diverse, desiccation-tolerant (DT) taxa, including, e.g., late embryogenesis abundant proteins (LEA) and reactive oxygen species scavengers. This up-regulation is observed in DT resurrection plants, mosses, and green algae most closely related to these Embryophytes. Here we test whether this same suite of protective genes is up-regulated during desiccation in even more distantly related DT green algae, and, importantly, whether that up-regulation is unique to DT algae or also occurs in a desiccation-intolerant relative. We used three closely related aquatic and desert-derived green microalgae in the family Scenedesmaceae and capitalized on extraordinary desiccation tolerance in two of the species, contrasting with desiccation intolerance in the third. We found that during desiccation, all three species increased expression of common protective genes. The feature distinguishing gene expression in DT algae, however, was extensive down-regulation of gene expression associated with diverse metabolic processes during the desiccation time course, suggesting a switch from active growth to energy-saving metabolism. This widespread downshift did not occur in the desiccation-intolerant taxon. These results show that desiccation-induced up-regulation of expression of protective genes may be necessary but is not sufficient to confer desiccation tolerance. The data also suggest that desiccation tolerance may require induced protective mechanisms operating in concert with massive down-regulation of gene expression controlling numerous other aspects of metabolism.
Rhizosphere heterogeneity shapes abundance and activity of sulfur-oxidizing bacteria in vegetated salt marsh sediments

(Frontiers Media, 2014-06-23) Thomas, François ; Giblin, Anne E. ; Cardon, Zoe G. ; Sievert, Stefan M.

Salt marshes are highly productive ecosystems hosting an intense sulfur (S) cycle, yet little is known about S-oxidizing microorganisms in these ecosystems. Here, we studied the diversity and transcriptional activity of S-oxidizers in salt marsh sediments colonized by the plant Spartina alterniflora, and assessed variations with sediment depth and small-scale compartments within the rhizosphere. We combined next-generation amplicon sequencing of 16S rDNA and rRNA libraries with phylogenetic analyses of marker genes for two S-oxidation pathways (soxB and rdsrAB). Gene and transcript numbers of soxB and rdsrAB phylotypes were quantified simultaneously, using newly designed (RT)-qPCR assays. We identified a diverse assemblage of S-oxidizers, with Chromatiales and Thiotrichales being dominant. The detection of transcripts from S-oxidizers was mostly confined to the upper 5 cm sediments, following the expected distribution of root biomass. A common pool of species dominated by Gammaproteobacteria transcribed S-oxidation genes across roots, rhizosphere, and surrounding sediment compartments, with rdsrAB transcripts prevailing over soxB. However, the root environment fine-tuned the abundance and transcriptional activity of the S-oxidizing community. In particular, the global transcription of soxB was higher on the roots compared to mix and rhizosphere samples. Furthermore, the contribution of Epsilonproteobacteria-related S-oxidizers tended to increase on Spartina roots compared to surrounding sediments. These data shed light on the under-studied oxidative part of the sulfur cycle in salt marsh sediments and indicate small-scale heterogeneities are important factors shaping abundance and potential activity of S-oxidizers in the rhizosphere.
Diel plant water use and competitive soil cation exchange interact to enhance NH4+ and K+ availability in the rhizosphere

(Springer, 2016-11-12) Espeleta, Javier F. ; Cardon, Zoe G. ; Mayer, K. Ulrich ; Neumann, Rebecca B.

Hydro-biogeochemical processes in the rhizosphere regulate nutrient and water availability, and thus ecosystem productivity. We hypothesized that two such processes often neglected in rhizosphere models — diel plant water use and competitive cation exchange — could interact to enhance availability of K+ and NH4+, both high-demand nutrients. A rhizosphere model with competitive cation exchange was used to investigate how diel plant water use (i.e., daytime transpiration coupled with no nighttime water use, with nighttime root water release, and with nighttime transpiration) affects competitive ion interactions and availability of K+ and NH4+. Competitive cation exchange enabled low-demand cations that accumulate against roots (Ca2+, Mg2+, Na+) to desorb NH4+ and K+ from soil, generating non-monotonic dissolved concentration profiles (i.e. ‘hotspots’ 0.1–1 cm from the root). Cation accumulation and competitive desorption increased with net root water uptake. Daytime transpiration rate controlled diel variation in NH4+ and K+ aqueous mass, nighttime water use controlled spatial locations of ‘hotspots’, and day-to-night differences in water use controlled diel differences in ‘hotspot’ concentrations. Diel plant water use and competitive cation exchange enhanced NH4+ and K+ availability and influenced rhizosphere concentration dynamics. Demonstrated responses have implications for understanding rhizosphere nutrient cycling and plant nutrient uptake.

Cardon Zoe G.

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