Publications

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    Haiwei Luo, Mary Ann Moran
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    ABSTRACT: Members of the Roseobacter clade are equipped with a tremendous diversity of metabolic capabilities, which in part explains their success in so many different marine habitats. Ideas on how this diversity evolved and is maintained are reviewed, focusing on recent evolutionary studies exploring the timing and mechanisms of Roseobacter ecological diversification. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Microbiology and molecular biology reviews: MMBR 12/2014; 78(4):573-587. · 12.59 Impact Factor
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    Haiwei Luo
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    ABSTRACT: Planktonic bacterial lineages with streamlined genomes are prevalent in the ocean. The base composition of their DNA is often highly biased towards low G+C content, a possible source of systematic error in phylogenetic reconstruction. A total of 228 orthologous protein families were sampled that are shared among major lineages of Alphaproteobacteria, including the marine free-living SAR11 clade and the obligate endosymbiotic Rickettsiales. These two ecologically distinct lineages share genome sizes of <1.5 Mbp and genomic G+C content of <30%. Statistical analyses showed that only 28 protein families are composition-homogeneous, whereas the other 200 families significantly violate the composition-homogeneous assumption included in most phylogenetic methods. RAxML analysis based on the concatenation of 24 ribosomal proteins that fall into the heterogeneous protein category clustered the SAR11 and Rickettsiales lineages at the base of the Alphaproteobacteria tree, whereas that based on the concatenation of 28 homogeneous proteins (including 19 ribosomal proteins) disassociated the lineages and placed SAR11 at the base of the non-endosymbiotic lineages. When the two data sets were concatenated, only a model that accounted for compositional bias yielded a tree identical to the tree built with composition-homogeneous proteins. Ancestral genome analysis suggests that the first evolved SAR11 cell had a small genome streamlined from its ancestor by a factor of two and coinciding with an ecological transition, followed by further gradual streamlining towards the extant SAR11 populations.The ISME Journal advance online publication, 28 November 2014; doi:10.1038/ismej.2014.227.
    The ISME Journal 11/2014; · 8.95 Impact Factor
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    ABSTRACT: Corallimorpharia is a small Order of skeleton-less animals that is closely related to the reef-building corals (Scleractinia) and of fundamental interest in the context of understanding the potential impacts of climate change in the future on coral reefs. The relationship between the nominal Orders Corallimorpharia and Scleractinia is controversial - the former is either the closest outgroup to the Scleractinia or, alternatively is derived from corals via skeleton loss. This latter scenario, the "naked coral" hypothesis, is strongly supported by analyses based on mitochondrial protein sequences, whereas the former is equally strongly supported by analyses of mitochondrial (mt) nucleotide sequences. The "naked coral" hypothesis seeks to link skeleton loss in the putative ancestor of corallimorpharians with a period of elevated oceanic CO2 during the Cretaceous, leading to the idea that these skeleton-less animals may be harbingers for the fate of coral reefs under global climate change. In an attempt to better understand their evolutionary relationships, we examined mitochondrial genome organization in a representative range (12 species, representing 3 of the 4 extant families) of corallimorpharians and compared these patterns to other Hexacorallia. The most surprising finding was that mt genome organization in Corallimorphus profundus, a deep-water species that is the most scleractinian-like of all corallimorpharians on the basis of morphology, was much more similar to the common scleractinian pattern than to those of other corallimorpharians. This finding is consistent with the idea that C. profundus represents a key position in the coral <-> corallimorpharian transition.
    Genome Biology and Evolution 04/2014; · 4.76 Impact Factor
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    ABSTRACT: Strain HIMB11 is a planktonic marine bacterium isolated from coastal seawater in Kaneohe Bay, Oahu, Hawaii belonging to the ubiquitous and versatile Roseobacter clade of the alphaproteobacterial family Rhodobacteraceae. Here we describe the preliminary characteristics of strain HIMB11, including annotation of the draft genome sequence and comparative genomic analysis with other members of the Roseobacter lineage. The 3,098,747 bp draft genome is arranged in 34 contigs and contains 3,183 protein-coding genes and 54 RNA genes. Phylogenomic and 16S rRNA gene analyses indicate that HIMB11 represents a unique sublineage within the Roseobacter clade. Comparison with other publicly available genome sequences from members of the Roseobacter lineage reveals that strain HIMB11 has the genomic potential to utilize a wide variety of energy sources (e.g. organic matter, reduced inorganic sulfur, light, carbon monoxide), while possessing a reduced number of substrate transporters.
    Standards in Genomic Sciences 02/2014; 9(3). · 3.17 Impact Factor
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    ABSTRACT: Previous studies based on analysis of amoA, 16S ribosomal RNA or accA gene sequences have established that marine Thaumarchaeota fall into two phylogenetically distinct groups corresponding to shallow- and deep-water clades, but it is not clear how water depth interacts with other environmental factors, including light, temperature and location, to affect this pattern of diversification. Earlier studies focused on single-gene distributions were not able to link phylogenetic structure to other aspects of functional adaptation. Here, we analyzed the genome content of 46 uncultivated single Thaumarchaeota cells sampled from epi- and mesopelagic waters of subtropical, temperate and polar oceans. Phylogenomic analysis showed that populations diverged by depth, as expected, and that mesopelagic populations from different locations were well mixed. Functional analysis showed that some traits, including putative DNA photolyase and catalase genes that may be related to adaptive mechanisms to reduce light-induced damage, were found exclusively in members of the epipelagic clade. Our analysis of partial genomes has thus confirmed the depth differentiation of Thaumarchaeota populations observed previously, consistent with the distribution of putative mechanisms to reduce light-induced damage in shallow- and deep-water populations.The ISME Journal advance online publication, 7 November 2013; doi:10.1038/ismej.2013.202.
    The ISME Journal 02/2014; 8:732-736. · 8.95 Impact Factor
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    ABSTRACT: The vast majority of surface ocean bacteria are uncultivated. Compared with their cultured relatives, they frequently exhibit a streamlined genome, reduced G+C content and distinct gene repertoire. These genomic traits are relevant to environmental adaptation, and have generally been thought to become fixed in marine bacterial populations through selection. Using single-cell genomics, we sequenced four uncultivated cells affiliated with the ecologically relevant Roseobacter clade and used a composition-heterogeneous Bayesian phylogenomic model to resolve these single-cell genomes into a new clade. This lineage has no representatives in culture, yet accounts for ∼35% of Roseobacters in some surface ocean waters. Analyses of multiple genomic traits, including genome size, G+C content and percentage of noncoding DNA, suggest that these single cells are representative of oceanic Roseobacters but divergent from isolates. Population genetic analyses showed that substitution of physicochemically dissimilar amino acids and replacement of G+C-rich to G+C-poor codons are accelerated in the uncultivated clade, processes that are explained equally well by genetic drift as by the more frequently invoked explanation of natural selection. The relative importance of drift vs selection in this clade, and perhaps in other marine bacterial clades with streamlined G+C-poor genomes, remains unresolved until more evidence is accumulated.The ISME Journal advance online publication, 23 January 2014; doi:10.1038/ismej.2013.248.
    The ISME Journal 01/2014; · 8.95 Impact Factor
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    ABSTRACT: A fundamental question in marine microbial ecology is how microbes adapt to ocean environments. Although numerically dominant populations are typically considered more successful, higher census population sizes (Nc) do not equate directly to a greater capability for adaptation. Instead, effective population size (Ne) determines the fate of deleterious and favourable mutations, and thus is a key parameter for determining the adaptive potential of a population. In the case of the SAR11 and Roseobacter lineages, two abundant heterotrophic bacteria in ocean surface waters with contrasting life history strategies, culture-independent population surveys suggest that SAR11s have greater Nc than Roseobacters. To determine relative Ne, we compared the ratio of nonsynonymous to synonymous substitution rates (ω) of recently diverged lineages of these taxa. Values of ω associated with several of the Roseobacter subclades were lower than for SAR11 subclades, suggesting greater Ne in these cases. Most Roseobacter lineages also had smaller ω values compared with an atypical basal Roseobacter lineage with a large Nc. This finding provides insight into variability in Ne across two important marine bacterial lineages, and provides an evolutionary context for considering how heterotrophic marine bacteria may differ in their ability to adapt to changing ocean habitats.
    Environmental Microbiology Reports 11/2013; 6(2):167–172. · 3.26 Impact Factor
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    Haiwei Luo, Mary Ann Moran
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    ABSTRACT: Uncovering the metabolic capabilities of microbes is key to understanding global energy flux and nutrient transformations. Since the vast majority of environmental microorganisms are uncultured, metagenomics has become an important tool to genotype the microbial community. This study uses a recently developed computational method to confidently assign metagenomic reads to microbial clades without the requirement of metagenome assembly by comparing the evolutionary pattern of nucleotide sequences at non-synonymous sites between metagenomic and orthologous reference genes. We found evidence for new, ecologically relevant metabolic pathways in several lineages of surface ocean bacterioplankton using the Global Ocean Survey (GOS) metagenomic data, including assimilatory sulfate reduction and alkaline phosphatase capabilities in the alphaproteobacterial SAR11 clade, and proteorhodopsin-like genes in the cyanobacterial genus Prochlorococcus. These findings raise new hypotheses about microbial roles in energy flux and organic matter transformation in the ocean.
    Environmental Microbiology Reports 10/2013; 5(5):686-696. · 3.26 Impact Factor
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    ABSTRACT: Planktonic bacteria dominate surface ocean biomass and influence global biogeochemical processes, but remain poorly characterized owing to difficulties in cultivation. Using large-scale single cell genomics, we obtained insight into the genome content and biogeography of many bacterial lineages inhabiting the surface ocean. We found that, compared with existing cultures, natural bacterioplankton have smaller genomes, fewer gene duplications, and are depleted in guanine and cytosine, noncoding nucleotides, and genes encoding transcription, signal transduction, and noncytoplasmic proteins. These findings provide strong evidence that genome streamlining and oligotrophy are prevalent features among diverse, free-living bacterioplankton, whereas existing laboratory cultures consist primarily of copiotrophs. The apparent ubiquity of metabolic specialization and mixotrophy, as predicted from single cell genomes, also may contribute to the difficulty in bacterioplankton cultivation. Using metagenome fragment recruitment against single cell genomes, we show that the global distribution of surface ocean bacterioplankton correlates with temperature and latitude and is not limited by dispersal at the time scales required for nucleotide substitution to exceed the current operational definition of bacterial species. Single cell genomes with highly similar small subunit rRNA gene sequences exhibited significant genomic and biogeographic variability, highlighting challenges in the interpretation of individual gene surveys and metagenome assemblies in environmental microbiology. Our study demonstrates the utility of single cell genomics for gaining an improved understanding of the composition and dynamics of natural microbial assemblages.
    Proceedings of the National Academy of Sciences 06/2013; · 9.81 Impact Factor
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    ABSTRACT: Proteorhodopsin (PR), a ubiquitous membrane photoprotein in marine environments, acts as a light-driven proton pump and can provide energy for bacterial cellular metabolism. However, knowledge of factors that regulate PR gene expression in different bacteria remains strongly limited. Here, experiments with Vibrio sp. AND4 showed that PR phototrophy promoted survival only in cells from stationary phase and not in actively growing cells. PR gene expression was tightly regulated, with very low values in exponential phase, a pronounced peak at the exponential/stationary phase intersection, and a marked decline in stationary phase. Thus, PR gene expression at the entry into stationary phase preceded, and could therefore largely explain, the stationary phase light-induced survival response in AND4. Further experiments revealed nutrient limitation, not light exposure, regulated this differential PR expression. Screening of available marine vibrios showed that the PR gene, and thus the potential for PR phototrophy, is found in at least three different clusters in the genus Vibrio. In an ecological context, our findings suggest that some PR-containing bacteria adapted to the exploitation of nutrient-rich micro-environments rely on a phase of relatively slowly declining resources to mount a cellular response preparing them for adverse conditions dispersed in the water column.
    Environmental Microbiology 01/2013; · 6.24 Impact Factor
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    ABSTRACT: ABSTRACT Marine bacteria in the Roseobacter and SAR11 lineages successfully exploit the ocean habitat, together accounting for ~40% of bacteria in surface waters, yet have divergent life histories that exemplify patch-adapted versus free-living ecological roles. Here, we use a phylogenetic birth-and-death model to understand how genome content supporting different life history strategies evolved in these related alphaproteobacterial taxa, showing that the streamlined genomes of free-living SAR11 were gradually downsized from a common ancestral genome only slightly larger than the extant members (~2,000 genes), while the larger and variably sized genomes of roseobacters evolved along dynamic pathways from a sizeable common ancestor (~8,000 genes). Genome changes in the SAR11 lineage occurred gradually over ~800 million years, whereas Roseobacter genomes underwent more substantial modifications, including major periods of expansion, over ~260 million years. The timing of the first Roseobacter genome expansion was coincident with the predicted radiation of modern marine eukaryotic phytoplankton of sufficient size to create nutrient-enriched microzones and is consistent with present-day ecological associations between these microbial groups. We suggest that diversification of red-lineage phytoplankton is an important driver of divergent life history strategies among the heterotrophic bacterioplankton taxa that dominate the present-day ocean. IMPORTANCE One-half of global primary production occurs in the oceans, and more than half of this is processed by heterotrophic bacterioplankton through the marine microbial food web. The diversity of life history strategies that characterize different bacterioplankton taxa is an important subject, since the locations and mechanisms whereby bacteria interact with seawater organic matter has effects on microbial growth rates, metabolic pathways, and growth efficiencies, and these in turn affect rates of carbon mineralization to the atmosphere and sequestration into the deep sea. Understanding the evolutionary origins of the ecological strategies that underlie biochemical interactions of bacteria with the ocean system, and which scale up to affect globally important biogeochemical processes, will improve understanding of how microbial diversity is maintained and enable useful predictions about microbial response in the future ocean.
    mBio 01/2013; 4(4). · 6.88 Impact Factor
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    Haiwei Luo, Austin L Hughes
    Molecular Systems Biology 11/2012; 8:625. · 11.34 Impact Factor
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    ABSTRACT: A typical marine bacterial cell in coastal seawater contains only ∼200 molecules of mRNA, each of which lasts only a few minutes before being degraded. Such a surprisingly small and dynamic cellular mRNA reservoir has important implications for understanding the bacterium's responses to environmental signals, as well as for our ability to measure those responses. In this perspective, we review the available data on transcript dynamics in environmental bacteria, and then consider the consequences of a small and transient mRNA inventory for functional metagenomic studies of microbial communities.
    The ISME Journal 08/2012; · 8.95 Impact Factor
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    ABSTRACT: Evolutionary relationships among placental mammalian orders have been controversial. Whole genome sequencing and new computational methods offer opportunities to resolve the relationships among 10 genomes belonging to the mammalian orders Primates, Rodentia, Carnivora, Perissodactyla and Artiodactyla. By application of the double cut and join distance metric, where gene order is the phylogenetic character, we computed genomic distances among the sampled mammalian genomes. With a marsupial outgroup, the gene order tree supported a topology in which Rodentia fell outside the cluster of Primates, Carnivora, Perissodactyla, and Artiodactyla. Results of breakpoint reuse rate and synteny block length analyses were consistent with the prediction of random breakage model, which provided a diagnostic test to support use of gene order as an appropriate phylogenetic character in this study. We discussed the influence of rate differences among lineages and other factors that may contribute to different resolutions of mammalian ordinal relationships by different methods of phylogenetic reconstruction.
    Molecular Phylogenetics and Evolution 08/2012; 65(3):871-82. · 4.07 Impact Factor
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    Haiwei Luo
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    ABSTRACT: Bacteria consume dissolved organic matter (DOM) through hydrolysis, transport and intracellular metabolism, and these activities occur in distinct subcellular localizations. Bacterial protein subcellular localizations for several major marine bacterial groups were predicted using genomic, metagenomic and metatranscriptomic data sets following modification of MetaP software for use with partial gene sequences. The most distinct pattern of subcellular localization was found for Bacteroidetes, whose genomes were substantially enriched with outer membrane and extracellular proteins but depleted of inner membrane proteins compared with five other taxa (SAR11, Roseobacter, Synechococcus, Prochlorococcus, oligotrophic marine Gammaproteobacteria). When subcellular localization patterns were compared between genes and transcripts, three taxa had expression biased toward proteins localized to cell locations outside of the cytosol (SAR11, Roseobacter, and Synechococcus), as expected based on the importance of carbon and nutrient acquisition in an oligotrophic ocean, but two taxa did not (oligotrophic marine Gammaproteobacteria and Bacteroidetes). Diel variations in the fraction and putative gene functions of transcripts encoding inner membrane and periplasmic proteins compared to cytoplasmic proteins suggest a close coupling of photosynthetic extracellular release and bacterial consumption, providing insights into interactions between phytoplankton, bacteria, and DOM.
    Applied and Environmental Microbiology 07/2012; 78(18):6550-7. · 3.95 Impact Factor
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    ABSTRACT: Understanding of the ecological roles and evolutionary histories of marine bacterial taxa can be complicated by mismatches in genome content between wild populations and their better-studied cultured relatives. We used computed patterns of non-synonymous (amino acid-altering) nucleotide diversity in marine metagenomic data to provide high-confidence identification of DNA fragments from uncultivated members of the Roseobacter clade, an abundant taxon of heterotrophic marine bacterioplankton in the world's oceans. Differences in gene stoichiometry in the Global Ocean Survey metagenomic data set compared with 39 sequenced isolates indicated that natural Roseobacter populations differ systematically in several genomic attributes from their cultured representatives, including fewer genes for signal transduction and cell surface modifications but more genes for Sec-like protein secretion systems, anaplerotic CO(2) incorporation, and phosphorus and sulfate uptake. Several of these trends match well with characteristics previously identified as distinguishing r- versus K-selected ecological strategies in bacteria, suggesting that the r-strategist model assigned to cultured roseobacters may be less applicable to their free-living oceanic counterparts. The metagenomic Roseobacter DNA fragments revealed several traits with evolutionary histories suggestive of horizontal gene transfer from other marine bacterioplankton taxa or viruses, including pyrophosphatases and glycosylation proteins.
    Environmental Microbiology 08/2011; 14(1):41-51. · 6.24 Impact Factor
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    ABSTRACT: Several isolates of the marine cyanobacterial genus Prochlorococcus have smaller genome sizes than those of the closely related genus Synechococcus. In order to test whether loss of protein-coding genes has contributed to genome size reduction in Prochlorococcus, we reconstructed events of gene family evolution over a strongly supported phylogeny of 12 Prochlorococcus genomes and 9 Synechococcus genomes. Significantly, more events both of loss of paralogs within gene families and of loss of entire gene families occurred in Prochlorococcus than in Synechococcus. The number of nonancestral gene families in genomes of both genera was positively correlated with the extent of genomic islands (GIs), consistent with the hypothesis that horizontal gene transfer (HGT) is associated with GIs. However, even when only isolates with comparable extents of GIs were compared, significantly more events of gene family loss and of paralog loss were seen in Prochlorococcus than in Synechococcus, implying that HGT is not the primary reason for the genome size difference between the two genera.
    Molecular Biology and Evolution 04/2011; 28(10):2751-60. · 14.31 Impact Factor
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    ABSTRACT: The biochemical composition of dissolved organic phosphorus (DOP) in the ocean is dominated by phosphoesters (C-O-P and C-O-P-O-C bonds), which are hydrolyzed by a diverse group of alkaline phosphatases (PhoA, PhoD, PhoX), and by phosphonates (C-P bond), which are degraded by C-P lyases and hydrolases. We designed a bioinformatics pipeline and a statistical approach to recover and analyze the alkaline phosphatase and phosphonate utilization genes from a metagenomic database derived from water samples collected from 7 depths (between 10 and 4000 m) in the oligotrophic North Pacific Subtropical Gyre. The alkaline phosphatase genes phoD and phoX were more abundant than phoA in the euphotic zone (10–130 m) and in deep waters (500–4000 m). The C-P lyase genes were most abundant in the euphotic zone at 70 m and were rare in deep water (≥500 m) where phosphate concentrations were relatively high. These observations indicate that phosphonates are utilized primarily as a phosphorus source by bacterial C-P lyases; this is consistent with the observation that C-P lyase genes are part of the pho regulon which is expressed upon phosphorus limitation. In contrast, C-P hydrolase and alkaline phosphatase genes were often more abundant in deep waters, indicating that DOP serves mainly as a carbon and energy source in phosphate-rich deep waters which are depleted in bioavailable dissolved organic matter (DOM). The observed differences in depth distributions and presumed functions of C-P lyase and hydrolase genes indicate variability in the chemical composition of phosphonates between the euphotic zone and deep waters.
    Aquatic Microbial Ecology 01/2011; 62:61-69. · 2.04 Impact Factor
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    ABSTRACT: Bacterial intergenic spacers are non-coding genomic regions enriched with cis-regulatory elements for gene expression. A population genetics approach was used to investigate the evolutionary force shaping the genetic diversity of intergenic spacers among 13 genomes of group A streptococcus (GAS). Analysis of 590 genes and their linked 5' intergenic spacers showed reduced nucleotide diversity in spacers compared to synonymous nucleotide diversity in protein-coding regions, suggestive of past purifying selection on spacers. Certain spacers showed elevated nucleotide diversity indicative of past homologous recombination with divergent genotypes. In addition, analysis of the difference between mean nucleotide difference and number of segregating sites showed evidence of an excess of rare variants both at nonsynonymous sites in genes and at sites in spacers, which is evidence that there are numerous slightly deleterious variants in GAS populations with potential effects on both protein sequences and gene expression.
    Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 11/2010; 11(2):343-8. · 3.22 Impact Factor
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    ABSTRACT: In recent years, gene order data has attracted increasing attention from both biologists and computer scientists as a new type of data for phylogenetic analysis. If gene orders are viewed as one character with a large number of states, traditional bootstrap procedures cannot be applied. Researchers began to use a jackknife resampling method to assess the quality of gene order phylogenies. In this paper, we design and conduct a set of experiments to validate the performance of this jackknife procedure and provide discussions on how to conduct it properly. Our results show that jackknife is very useful to determine the confidence level of a phylogeny obtained from gene orders and a jackknife rate of 40% should be used. However, although a branch with support value of 85% can be trusted, low support branches require careful investigation before being discarded. Our experiments show that jackknife is indeed necessary and useful for gene order data, yet some caution should be taken when the results are interpreted.
    BMC Bioinformatics 04/2010; 11:168. · 3.02 Impact Factor

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