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Publications

When it comes to interdisciplinary collaboration, the titles of GLBRC publications speak for themselves. Each new year of operation has seen more publications from multiple labs that span the four Research Areas, accelerating the Center's production of the basic research that generates technology to convert cellulosic biomass to advanced biofuels.

Publications

Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan

Markus Pauly; Kenneth Keegstra

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2016

Xyloglucan (XyG) is a matrix polysaccharide that is present in the cell walls of all land plants. It consists of a beta-1,4-linked glucan backbone that is further substituted with xylosyl residues. These xylosyl residues can be further substituted with other glycosyl and nonglycosyl substituents that vary depending on the plant family and specific tissue. Advances in plant mutant isolation and characterization, functional genomics, and DNA sequencing have led to the identification of nearly all transferases and synthases necessary to synthesize XyG. Thus, in terms of the molecular mechanisms of plant cell wall polysaccharide biosynthesis, XyG is the most well understood. However, much remains to be learned about the molecular mechanisms of polysaccharide assembly and the regulation of these processes. Knowledge of the XyG biosynthetic machinery allows the XyG structure to be tailored in planta to ascertain the functions of this polysaccharide and its substituents in plant growth and interactions with the environment. Expected final online publication date for the Annual Review of Plant Biology Volume 67 is April 29, 2016. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.

Cell wall composition and biomass recalcitrance differences within a genotypically diverse set of Brachypodium distachyon inbred lines

Cynthia L. Cass; Anastasiya A. Lavell; Nicholas Santoro; Cliff E. Foster; Steven D. Karlen; Rebecca A. Smith; John Ralph; David F. Garvin; John C. Sedbrook

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2016

Cellulose-enriched microbial communities from leaf-cutter ant (Atta colombica) refuse dumps vary in taxonomic composition and degradation ability

Gina R. Lewin; Amanda L. Johnson; Rolando D. Soto; Kailene Perry; Adam J. Book; Heidi A. Horn; Adrian A. Pinto-Tomas; Cameron R. Currie

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2016

Deconstruction of the cellulose in plant cell walls is critical for carbon flow through ecosystems and for the production of sustainable cellulosic biofuels. Our understanding of cellulose deconstruction is largely limited to the study of microbes in isolation, but in nature, this process is driven by microbes within complex communities. In Neotropical forests, microbes in leaf-cutter ant refuse dumps are important for carbon turnover. These dumps consist of decaying plant material and a diverse bacterial community, as shown here by electron microscopy. To study the portion of the community capable of cellulose degradation, we performed enrichments on cellulose using material from five Atta colombica refuse dumps. The ability of enriched communities to degrade cellulose varied significantly across refuse dumps. 16S rRNA gene amplicon sequencing of enriched samples identified that the community structure correlated with refuse dump and with degradation ability. Overall, samples were dominated by Bacteroidetes, Gammaproteobacteria, and Betaproteobacteria. Half of abundant operational taxonomic units (OTUs) across samples were classified within genera containing known cellulose degraders, including Acidovorax, the most abundant OTU detected across samples, which was positively correlated with cellulolytic ability. A representative Acidovorax strain was isolated, but did not grow on cellulose alone. Phenotypic and compositional analyses of enrichment cultures, such as those presented here, help link community composition with cellulolytic ability and provide insight into the complexity of community-based cellulose degradation.

Characterizing phenol–formaldehyde adhesive cure chemistry within the wood cell wall

Daniel J. Yelle; John Ralph

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2016

Adhesive bonding of wood using phenol–formaldehyde remains the industrial standard in wood product bond durability. Not only does this adhesive infiltrate the cell wall, it also is believed to form primary bonds with wood cell wall polymers, particularly guaiacyl lignin. However, the mechanism by which phenol–formaldehyde adhesive integrally interacts and bonds to lignin within the cell wall remains unclear. We used recently developed solubilization methodologies in conjunction with two-dimensional 1H–13C solution-state NMR spectroscopy of ball-milled pine earlywood and latewood bonded assemblies to characterize the chemical modification of wood cell wall polymers after phenol–formaldehyde curing at various cooking times. The results showed that the highly alkaline resin at 140 °C decreased the frequency of the principal arylglycerol-β-aryl ether interunit linkage by eighty percent in earlywood and by twenty percent in latewood. The presence of newly formed diarylmethanes between guaiacyl lignin units and phenolic methylols was confirmed via NMR spectra of the aliphatic methylene and aromatic regions. The phenol–formaldehyde cure chemistry showed that o–p methylene bridges dominated in both earlywood and latewood cell walls, but the propensity of p–p substitution is higher in the latewood cell wall. Our results provide evidence for a simultaneous wood polymer degradation and guaiacyl unit C5 bond formation that occurs during phenol–formaldehyde curing. This competition may be necessary for developing good bond durability between the adhesive and wood.

Climate-smart soils

Keith Paustian; Johannes Lehmann; Stephen Ogle; David Reay; Philip Robertson; Pete Smith

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2016

Soils are integral to the function of all terrestrial ecosystems and to food and fibre production. An overlooked aspect of soils is their potential to mitigate greenhouse gas emissions. Although proven practices exist, the implementation of soil-based greenhouse gas mitigation activities are at an early stage and accurately quantifying emissions and reductions remains a substantial challenge. Emerging research and information technology developments provide the potential for a broader inclusion of soils in greenhouse gas policies. Here we highlight ‘state of the art’ soil greenhouse gas research, summarize mitigation practices and potentials, identify gaps in data and understanding and suggest ways to close such gaps through new research, technology and collaboration.

CO2 uptake is offset by CH4 and N2O emissions in a poplar short-rotation coppice

Terenzio Zenone; Donatella Zona; Ilya Gelfand; Bert Gielen; Marta Camino-Serrano; Reinhart Ceulemans

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2016

The need for renewable energy sources will lead to a considerable expansion in the planting of dedicated fast-growing biomass crops across Europe. These are commonly cultivated as short-rotation coppice (SRC), and currently poplar (Populus spp.) is the most widely planted. In this study, we report the greenhouse gas (GHG) fluxes of carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O) measured using eddy covariance technique in an SRC plantation for bioenergy production. Measurements were made during the period 2010–2013, that is, during the first two rotations of the SRC. The overall GHG balance of the 4 years of the study was an emission of 1.90 (±1.37) Mg CO2eq ha−1; this indicated that soil trace gas emissions offset the CO2 uptake by the plantation. CH4 and N2O contributed almost equally to offset the CO2 uptake of −5.28 (±0.67) Mg CO2eq ha−1 with an overall emission of 3.56 (±0.35) Mg CO2eq ha−1 of N2O and of 3.53 (±0.85) Mg CO2eq ha−1 of CH4. N2O emissions mostly occurred during one single peak a few months after the site was converted to SRC; this peak comprised 44% of the total N2O loss during the two rotations. Accurately capturing emission events proved to be critical for deriving correct estimates of the GHG balance. The nitrogen (N) content of the soil and the water table depth were the two drivers that best explained the variability in N2O and CH4, respectively. This study underlines the importance of the ‘non-CO2 GHGs’ on the overall balance. Further long-term investigations of soil trace gas emissions should monitor the N content and the mineralization rate of the soil, as well as the microbial community, as drivers of the trace gas emissions.

Comparative genomics of biotechnologically important yeasts

Robert Riley; Sajeet Haridas; Kenneth H. Wolfe; Mariana R. Lopes; Chris T. Hittinger; Markus Goker; Asaf A. Salamov; Jennifer H. Wisecaver; Tanya M. Long; Christopher H. Calvey; Andrea L. Aerts; Keriie W. Barry; Cindy Choi; Alicia Clum; Aisling Y. Coughlan; Shweta Deshpande; Alexander P. Douglass; Sara J. Hanson; Hans-Peter Klenk; Kurt M. LaButti; Alla Lapidus; Erika A. Lindquist; Anna M. Lipzen; Jan P. Meier-Kolthoff; Robin A. Ohm; Robert P. Otillar; Jasmyn L. Pangilinan; Yi Peng; Antonis Rokas; Carlos A. Rosa; Carmen Scheuner; Andriy A. Sibirny; Jason C. Slot; J. B. Stielow; Hui Sun; Cletus P. Kurtzman; Meredith Blackwell; Igor V. Grigoriev; Thomas W. Jeffries

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2016

Ascomycete yeasts are metabolically diverse, with great potential for biotechnology. Here, we report the comparative genome analysis of 29 taxonomically and biotechnologically important yeasts, including 16 newly sequenced. We identify a genetic code change, CUG-Ala, in Pachysolen tannophilus in the clade sister to the known CUG-Ser clade. Our well-resolved yeast phylogeny shows that some traits, such as methylotrophy, are restricted to single clades, whereas others, such as l-rhamnose utilization, have patchy phylogenetic distributions. Gene clusters, with variable organization and distribution, encode many pathways of interest. Genomics can predict some biochemical traits precisely, but the genomic basis of others, such as xylose utilization, remains unresolved. Our data also provide insight into early evolution of ascomycetes. We document the loss of H3K9me2/3 heterochromatin, the origin of ascomycete mating-type switching, and panascomycete synteny at the MAT locus. These data and analyses will facilitate the engineering of efficient biosynthetic and degradative pathways and gateways for genomic manipulation.

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

Nicolas Bellora; Martin Moline; Marcia David-Palma; Marco A. Coelho; Chris T. Hittinger; Jose P. Sampaio; Paula Goncalves; Diego Libkind

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2016

BACKGROUND: The class Tremellomycete (Agaricomycotina) encompasses more than 380 fungi. Although there are a few edible Tremella spp., the only species with current biotechnological use is the astaxanthin-producing yeast Phaffia rhodozyma (Cystofilobasidiales). Besides astaxanthin, a carotenoid pigment with potent antioxidant activity and great value for aquaculture and pharmaceutical industries, P. rhodozyma possesses multiple exceptional traits of fundamental and applied interest. The aim of this study was to obtain, and analyze two new genome sequences of representative strains from the northern (CBS 7918T, the type strain) and southern hemispheres (CRUB 1149) and compre them to a previously published genome sequence (strain CBS 6938). Photoprotection and antioxidant related genes, as well as genes involved in sexual reproduction were analyzed. RESULTS: Both genomes had ca. 19 Mb and 6000 protein coding genes, similar to CBS 6938. Compared to other fungal genomes P. rhodozyma strains and other Cystofilobasidiales have the highest number of intron-containing genes and highest number of introns per gene. The Patagonian strain showed 4.4 % of nucleotide sequence divergence compared to the European strains which differed from each other by only 0.073 %. All known genes related to the synthesis of astaxanthin were annotated. A hitherto unknown gene cluster potentially responsible for photoprotection (mycosporines) was found in the newly sequenced P. rhodozyma strains but was absent in the non-mycosporinogenic strain CBS 6938. A broad battery of enzymes that act as scavengers of free radical oxygen species were detected, including catalases and superoxide dismutases (SODs). Additionally, genes involved in sexual reproduction were found and annotated. CONCLUSIONS: A draft genome sequence of the type strain of P. rhodozyma is now available, and comparison with that of the Patagonian population suggests the latter deserves to be assigned to a distinct variety. An unexpected genetic trait regarding high occurrence of introns in P. rhodozyma and other Cystofilobasidiales was revealed. New genomic insights into fungal homothallism were also provided. The genetic basis of several additional photoprotective and antioxidant strategies were described, indicating that P. rhodozyma is one of the fungi most well-equipped to cope with environmental oxidative stress, a factor that has probably contributed to shaping its genome.

Comparative productivity of alternative cellulosic bioenergy cropping systems in the North Central USA

Gregg R. Sanford; Lawrence G. Oates; Poonam Jasrotia; Kurt D. Thelen; Philip Robertson; Randall D. Jackson

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2016

Biofuels from lignocellulosic feedstocks have the potential to improve a wide range of ecosystem services while simultaneously reducing dependence on fossil fuels. Here, we report on the six-year production potential (above ground net primary production, ANPP), post-frost harvested biomass (yield), and gross harvest efficiency (GHE = yield/ANPP) of seven model bioenergy cropping systems in both southcentral Wisconsin (ARL) and southwest Michigan (KBS). The cropping systems studied were continuous corn (Zea mays L.), switchgrass (Panicum virgatum L.), giant miscanthus (Miscanthus × giganteus Greef & Deuter ex Hodkinson & Renvoize), hybrid poplar (Populus nigra × P. maximowiczii A. Henry ‘NM6’), a native grass mixture (5 sown species), an early successional community, and a restored prairie (18 sown species). Overall the most productive cropping systems were corn > giant miscanthus > and switchgrass, which were significantly more productive than native grasses ≈ restored prairie ≈ early successional ≈ and hybrid poplar, although some systems (e.g. hybrid poplar) differed significantly by location. Highest total ANPP was observed in giant miscanthus (35.2 ± 2.0 Mg ha−1 yr−1) at KBS during the sixth growing season. Six-year cumulative biomass yield from hybrid poplar at KBS (55.4 ± 1.3 Mg ha−1) was high but significantly lower than corn and giant miscanthus (65.5 ± 1.5, 65.2 ± 5.5 Mg ha−1, respectively). Hypothesized yield advantages of diversity in perennial cropping systems were not observed during this period. Harvested biomass yields were 60, 56, and 44% of ANPP for corn, perennial grass, and restored prairie, respectively, suggesting that relatively simple changes in agronomic management (e.g. harvest timing and harvest equipment modification) may provide significant gains in bioenergy crop yields. Species composition was an important determinant of GHE in more diverse systems. Results show that well-established, dedicated bioenergy crops are capable of producing as much biomass as corn stover, but with fewer inputs.

Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus

David Peris; Quinn Langdon; Ryan V. Moriarty; Kayla Sylvester; Martin Bontrager; Guillaume Charron; Jean-Baptiste LeDuc; Christian R. Landry; Diego Libkind; Chris T. Hittinger

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2016

Lager-style beers constitute the vast majority of the beer market, and yet, the genetic origin of the yeast strains that brew them has been shrouded in mystery and controversy. Unlike ale-style beers, which are generally brewed with Saccharomyces cerevisiae, lagers are brewed at colder temperatures with allopolyploid hybrids of Saccharomyces eubayanus x S. cerevisiae. Since the discovery of S. eubayanus in 2011, additional strains have been isolated from South America, North America, Australasia, and Asia, but only interspecies hybrids have been isolated in Europe. Here, using genome sequence data, we examine the relationships of these wild S. eubayanus strains to each other and to domesticated lager strains. Our results support the existence of a relatively low-diversity (π = 0.00197) lineage of S. eubayanus whose distribution stretches across the Holarctic ecozone and includes wild isolates from Tibet, new wild isolates from North America, and the S. eubayanus parents of lager yeasts. This Holarctic lineage is closely related to a population with higher diversity (π = 0.00275) that has been found primarily in South America but includes some widely distributed isolates. A second diverse South American population (π = 0.00354) and two early-diverging Asian subspecies are more distantly related. We further show that no single wild strain from the Holarctic lineage is the sole closest relative of lager yeasts. Instead, different parts of the genome portray different phylogenetic signals and ancestry, likely due to outcrossing and incomplete lineage sorting. Indeed, standing genetic variation within this wild Holarctic lineage of S. eubayanus is responsible for genetic variation still segregating among modern lager-brewing hybrids. We conclude that the relationships among wild strains of S. eubayanus and their domesticated hybrids reflect complex biogeographical and genetic processes.

Corn stover ethanol yield as affected by grain yield, Bt trait, and environment

Pavani Tumbalam; Kurt D. Thelen; Andrew Adkins; Bruce Dale; Venkatesh Balan; Christa Gunawan; Juan Gao

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2016

Literature values for glucose release from corn stover are highly variable which would likely result in tremendous variability in bio-refinery ethanol yield from corn stover feedstock. A relatively recent change in United States corn genetics is the inclusion of the Bacillus thuringiensis (Bt) trait, which now accounts for three-fourths of all US planted corn acreage. The objective of this study was to evaluate the effect of corn grain yield, inclusion of the Bt trait, and location environment on corn stover quality for subsequent ethanol conversion. Two hybrid pairs (each having a Bt and non-Bt near-isoline) were analyzed giving a total of 4 hybrids. In 2010 and 2011, field plots were located in Michigan at four lat- itudinal differing locations in four replicated plots at each location. Stover composition and enzymatic digestibility was analyzed and estimated ethanol yield (g g 1) was calculated based on hydrolyzable glucan and xylan levels. Analysis showed that there were no significant differences in total glucose or xylose levels nor in enzymatically hydrolyzable glucan and xylan concentrations between Bt corn stover and the non-Bt stover isolines. Regression analyses between corn grain yield (Mg ha 1) and corn stover ethanol yield (g g 1) showed an inverse relationship indicative of a photosynthate source-sink rela- tionship. Nevertheless, the quantity of stover produced was found to be more critical than the quality of stover produced in maximizing potential stover ethanol yield on a land area basis.

Cover crops have neutral effects on predator communities and biological control services in annual cellulosic bioenergy cropping systems

Aaron F. Fox; Tania N. Kim; Christine A. Bahlai; Megan Woltz; Claudio Gratton; Douglas A. Landis

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2016

Maize stover is beginning to be used as a cellulosic biofuel feedstock in the Midwestern United States; however, there are concerns that stover removal could result in increased soil erosion and loss of soil organic matter. Use of a winter cover crop following maize harvest has the potential to mitigate these impacts and may have additional benefits by providing continuous living cover in annual crop habitats leading to changes in insect predator communities and increased biocontrol services. However, cover crops may also be harvested in cellulosic biofuel systems, adding a disturbance event that may negatively affect biocontrol. We contrasted insect predator communities and their impacts in four potential bioenergy cropping systems in Michigan and Wisconsin (USA) during the 2013 and 2014 growing seasons. Two annual maize systems were harvested for grain and stover; one maize system included a cereal rye/Austrian winter pea cover crop. Two perennial systems, switchgrass and a mixed prairie grasses and forbs, were harvested in the fall for biomass. Predatory insect abundance and diversity were lower in both annual cropping systems than in the perennial cropping systems and the inclusion of the cover crop did not significantly alter these responses. Similarly, removal of sentinel insect egg prey was also lower in the annual versus perennial cropping systems, with no significant influence of cover crop. We also explored the potential for cover crops to harbor prey populations in the spring that might encourage oviposition by mobile predators and potentially lead to local population sources or sinks of predators depending on the timing and effect of cover crop harvest. We found that existing predator communities in the cover crop treatments effectively suppressed aphid population growth, limiting their attractiveness to mobile predators. While we found no significant positive or negative impacts of this cover crop system on biocontrol services, bioenergy cover cropping systems could be managed to increase multiple ecosystem services by altering cover crop identity, or timing of planting and harvest.

Design of cellulosic ethanol supply chains with regional depots

Rex T.L. Ng; Christos T. Maravelias

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2016

The conversion of lignocellulosic biomass to fuels has the potential to reduce our dependence on fossil fuels. To ensure biomass supply meets biofuel demand, it is necessary to have an effective biomass supply network. Toward this end, the concept of regional biomass processing depot, where biomass is pretreated and/or densified to a higher density intermediate, has been introduced to improve the performance of supply network in terms of costs and emissions. In this article, we develop a mixed-integer nonlinear programming model for the capacity and inventory planning problem of biofuels supply chain including depots. Importantly, the proposed model accounts for variable locations of depots, which is a subject that has not been studied in the literature. In addition, our models account for biomass selection and allocation, technology selection and capacity planning at depots and biorefineries, and biomass seasonality.

Designer lignins: harnessing the plasticity of lignification

Yaseen Mottiar; Ruben Vanholme; Wout Boerjan; John Ralph; Shawn D. Mansfield

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2016

Lignin is a complex polyphenolic constituent of plant secondary cell walls. Inspired largely by the recalcitrance of lignin to biomass processing, plant engineering efforts have routinely sought to alter lignin quantity, composition, and structure by exploiting the inherent plasticity of lignin biosynthesis. More recently, researchers are attempting to strategically design plants for increased degradability by incorporating monomers that lead to a lower degree of polymerisation, reduced hydrophobicity, fewer bonds to other cell wall constituents, or novel chemically labile linkages in the polymer backbone. In addition, the incorporation of value-added structures could help valorise lignin. Designer lignins may satisfy the biological requirement for lignification in plants while improving the overall efficiency of biomass utilisation.

Detection of short-term cropping system-induced changes to soil bacterial communities differs among four molecular characterization methods

David S. Duncan; Kelsea A. Jewell; Garret Suen; Randall D. Jackson

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2016

Perennial grass-based agroecosystems are under consideration as sustainable sources of bioenergy feedstocks. Establishing these systems on land previously used for conventional agricultural production is expected to dramatically alter the composition and functional capacity of their associated soil bacterial communities, but the rate at which these changes will occur is unclear. Methods for characterizing bacterial communities are both varied and useful for documenting different aspects of the soil microbiota and their dynamics during this transition. Here, we studied the soil-associated bacterial communities of continuous corn and restored prairies systems within a cropping systems experiment 2–4 years after establishment using 1) phospholipid fatty acid (PLFA) profiling, 2) shotgun metagenomic sequencing, 3) amplicon sequencing of the 16S rRNA gene and 4) sequencing of the nitrogen-cycling gene nosZ. All characterization methods discriminated the bacterial communities between the two cropping systems, but the largest differences were observed with PLFA profiling. Differences between the two cropping systems did not significantly increase during the study period. The community compositions described by sequence-based methods were mutually correlated, but were only weakly correlated to the composition described by PLFA profiling. Shotgun metagenomics detected a much higher abundance of Actinobacteria than amplicon sequencing and revealed more consistent changes between cropping systems over time. Cropping system and interannual effects on the ratios of biomarkers associated with Gram-negative and Gram-positive bacteria were entirely different for PLFAs, rRNA amplicons, and shotgun-sequenced 16S rRNA. Our findings highlight how soil bacterial community characterization methods differ in their detection of microbial community composition as a result of recent land use change.

Different functions of phylogenetically distinct bacterial complex I isozymes

Melanie A. Spero; Joshua R. Brickner; Jordan T. Mollet; Tippapha Pisithkul; Daniel Amador-Noguez; Timothy J. Donohue

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2016

NADH:quinone oxidoreductase (complex I) is a bioenergetic enzyme that transfers electrons from NADH to quinone, conserving the energy of this reaction by contributing to the proton motive force. While the importance of NADH oxidation to mitochondrial aerobic respiration is well documented, the contribution of complex I to the different electron transport chains of bacteria has only been tested in a few species. The discovery that individual bacteria contain phylogenetically distinct complex I enzymes begs the question of whether individual isozymes serve different functions. Here, we analyze the function of two phylogenetically distinct complex I isozymes in Rhodobacter sphaeroides, an α-proteobacterium that contains well-characterized electron transport chains. We report that complex I function is central to R. sphaeroides energy metabolism, since a strain lacking both complex I isozymes grew more slowly via aerobic respiration and had anaerobic growth defects. Several observations also led us to conclude that the two complex I isozymes are not functionally redundant. For example, the complex I isozyme typically found in α-proteobacteria (referred to as complex IA) is required for photoheterotrophic growth on carbon sources whose catabolism is predicted to produce reduced quinone, while the isozyme that is commonly present in γ-proteobacteria (complex IE) is required for photoheterotrophic growth on carbon sources whose catabolism produces high levels of NADH. Additionally, complex IA is required to produce wild type levels of H2, while complex IE is dispensable for this process. We propose that these findings illustrate specific roles of complex I isozymes in either NADH synthesis (complex IA) or NADH oxidation (complex IE) during phototrophic growth. Unlike the singular role of complex I in mitochondrial aerobic respiration, we predict that the phylogenetically-distinct complex I isozymes found across bacterial species have evolved to enhance function in their respective electron transport chains

Directed evolution reveals unexpected epistatic interactions that alter metabolic regulation and enable anaerobic xylose use by Saccharomyces cerevisiae

Trey K. Sato; Mary Tremaine; Lucas S. Parreiras; Alexander S. Herbert; Kevin S. Myers; Alan J. Higbee; Maria Sardi; Sean J. McIlwain; Irene M. Ong; Rebecca J. Breuer; Ragothaman Avanasi Narasimhan; Mick A. McGee; Quinn Dickinson; Alex La Reau; Dan Xie; Mingyuan Tian; Jeff S. Piotrowski; Jennifer L. Reed; Yaoping Zhang; Joshua J. Coon; Chris Todd Hittinger; Audrey P. Gasch; Robert Landick

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2016

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