Serres Margrethe H.

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Serres

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Margrethe H.

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Genomic analysis of carbon source metabolism of Shewanella oneidensis MR-1 : predictions versus experiments

(American Society for Microbiology, 2006-07) Serres, Margrethe H. ; Riley, Monica

Genomic sequences have been used to find the genetic foundation for carbon source metabolism in Shewanella oneidensis MR-1. Annotated S. oneidensis MR-1 gene products were examined for their sequence similarity to enzymes participating in pathways for utilization of carbon and energy as described in the BioCyc database (http://www.biocyc.org/) or in the primary literature. A picture emerges that relegates five- and six-carbon sugars to minor roles as carbon sources, whereas multiple pathways for utilization of up to three-carbon carbohydrates seem to be present. Capacity to utilize amino acids for carbon and energy is also present. A few contradictions emerged in which enzymes appear to be present by annotations but are not active in the cell according to physiological experiments. Annotations are based on close sequence similarity and will not reveal inactivity due to deleterious mutations or due to lack of coordination of regulation and transport. Genes for a few enzymes known by experiment to be active are not found in the genome. This may be due to extensive divergence after duplication or convergence of function in separate lines in evolution rendering activities undetectable by sequence similarity. To minimize false predictions from protein sequences, we have been conservative in predicting pathways. We did not predict any pathway when, although a partial pathway was seen it was composed largely of enzymes already accounted for in any other complete pathway. This is an example of how a biochemically oriented sequence analysis can generate questions and direct further experimental investigation.
Draft genome sequence of Desulfurobacterium sp. Strain AV08, a Thermophilic Chemolithoautotroph isolated from a deep-sea hydrothermal vent

(American Society for Microbiology, 2021-08-26) Skoog, Emilie J. ; Huber, Julie A. ; Serres, Margrethe H. ; Levesque, Alice ; Zeigler Allen, Lisa

A thermophilic chemolithoautotrophic bacterium was isolated from vent fluids at Axial Seamount, an active deep-sea volcano in the northeast Pacific Ocean. We present the draft genome sequence of Desulfurobacterium sp. strain AV08.
Evolution by leaps : gene duplication in bacteria

(BioMed Central, 2009-11-23) Serres, Margrethe H. ; Kerr, Alastair R. W. ; McCormack, Thomas J. ; Riley, Monica

Sequence related families of genes and proteins are common in bacterial genomes. In Escherichia coli they constitute over half of the genome. The presence of families and superfamilies of proteins suggest a history of gene duplication and divergence during evolution. Genome encoded protein families, their size and functional composition, reflect metabolic potentials of the organisms they are found in. Comparing protein families of different organisms give insight into functional differences and similarities. Equivalent enzyme families with metabolic functions were selected from the genomes of four experimentally characterized bacteria belonging to separate genera. Both similarities and differences were detected in the protein family memberships, with more similarities being detected among the more closely related organisms. Protein family memberships reflected known metabolic characteristics of the organisms. Differences in divergence of functionally characterized enzyme family members accounted for characteristics of taxa known to differ in those biochemical properties and capabilities. While some members of the gene families will have been acquired by lateral exchange and other former family members will have been lost over time, duplication and divergence of genes and functions appear to have been a significant contributor to the functional diversity of today’s microbes. Protein families seem likely to have arisen during evolution by gene duplication and divergence where the gene copies that have been retained are the variants that have led to distinct bacterial physiologies and taxa. Thus divergence of the duplicate enzymes has been a major process in the generation of different kinds of bacteria.
Large-scale comparative phenotypic and genomic analyses reveal ecological preferences of Shewanella species and identify metabolic pathways conserved at the genus level

( 2011-04-27) Rodrigues, Jorge L. M. ; Serres, Margrethe H. ; Tiedje, James M.

The use of comparative genomics among different microbiological species has increased substantially as sequence technologies become more affordable. However, efforts to fully link a genotype to its phenotype remain limited to the development of one mutant at the time. In this study, we provide a high throughput alternative to this limiting step by coupling comparative genomics to phenotype arrays for five sequenced Shewanella strains. Positive phenotypes were obtained for 441 nutrients (C, N, P, and S sources), with N-based compounds being the most utilized for all strains. Many genes and pathways predicted by genome analyses were confirmed with the comparative phenotype assay, and three degradation pathways believed to be missing in Shewanella were confirmed. A number of previously unknown gene products were predicted to be part of pathways or to have a function, expanding the number of gene targets for future genetic analyses. Ecologically, the comparative high throughput phenotype analysis provided insights into niche specialization within the five different strains. For example, Shewanella amazonensis strain SB2B, isolated from the Amazon River delta, was capable of utilizing 60 C compounds, whereas Shewanella sp. strain W3-18-1, from the deep marine sediment, utilized only 25 of them. In spite of the large number of nutrient sources yielding positive results, our study indicated that except for the N-sources they were not sufficiently informative to predict growth phenotypes from increasing evolutionary distances. Our results indicate the importance of phenotypic evaluation for confirming genome predictions. This strategy will accelerate the functional discovery of genes and provide an ecological framework for microbial genome sequencing projects.
Comparative systems biology across an evolutionary gradient within the Shewanella genus

( 2009-07) Konstantinidis, Konstantinos T. ; Serres, Margrethe H. ; Romine, Margaret F. ; Rodrigues, Jorge L. M. ; Auchtung, Jennifer ; McCue, Lee-Ann ; Lipton, Mary S. ; Obraztsova, Anna Y. ; Giometti, Carol S. ; Nealson, Kenneth H. ; Fredrickson, James K. ; Tiedje, James M.

To what extent genotypic differences translate to phenotypic variation remains a poorly understood issue of paramount importance for several cornerstone concepts of microbiology including the species definition. Here, we take advantage of the completed genomic sequences, expressed proteomic profiles, and physiological studies of ten closely related Shewanella strains and species to provide quantitative insights into this issue. Our analyses revealed that, despite extensive horizontal gene transfer within these genomes, the genotypic and phenotypic similarities among the organisms were generally predictable from their evolutionary relatedness. The power of the predictions depended on the degree of ecological specialization of the organisms evaluated. Using the gradient of evolutionary relatedness formed by these genomes, we were able to partly isolate the effect of ecology from that of evolutionary divergence and rank the different cellular functions in terms of their rates of evolution. Our ranking also revealed that whole-cell protein expression differences among these organisms when grown under identical conditions were relatively larger than differences at the genome level, suggesting that similarity in gene regulation and expression should constitute another important parameter for (new) species description. Collectively, our results provide important new information towards beginning a systems-level understanding of bacterial species and genera.
Gene fusions and gene duplications : relevance to genomic annotation and functional analysis

(BioMed Central, 2005-03-09) Serres, Margrethe H. ; Riley, Monica

Background: Escherichia coli a model organism provides information for annotation of other genomes. Our analysis of its genome has shown that proteins encoded by fused genes need special attention. Such composite (multimodular) proteins consist of two or more components (modules) encoding distinct functions. Multimodular proteins have been found to complicate both annotation and generation of sequence similar groups. Previous work overstated the number of multimodular proteins in E. coli. This work corrects the identification of modules by including sequence information from proteins in 50 sequenced microbial genomes. Results: Multimodular E. coli K-12 proteins were identified from sequence similarities between their component modules and non-fused proteins in 50 genomes and from the literature. We found 109 multimodular proteins in E. coli containing either two or three modules. Most modules had standalone sequence relatives in other genomes. The separated modules together with all the single (un-fused) proteins constitute the sum of all unimodular proteins of E. coli. Pairwise sequence relationships among all E. coli unimodular proteins generated 490 sequence similar, paralogous groups. Groups ranged in size from 92 to 2 members and had varying degrees of relatedness among their members. Some E. coli enzyme groups were compared to homologs in other bacterial genomes. Conclusion: The deleterious effects of multimodular proteins on annotation and on the formation of groups of paralogs are emphasized. To improve annotation results, all multimodular proteins in an organism should be detected and when known each function should be connected with its location in the sequence of the protein. When transferring functions by sequence similarity, alignment locations must be noted, particularly when alignments cover only part of the sequences, in order to enable transfer of the correct function. Separating multimodular proteins into module units makes it possible to generate protein groups related by both sequence and function, avoiding mixing of unrelated sequences. Organisms differ in sizes of groups of sequence-related proteins. A sample comparison of orthologs to selected E. coli paralogous groups correlates with known physiological and taxonomic relationships between the organisms.
A functional update of the Escherichia coli K-12 genome

(BioMed Central, 2001-08-20) Serres, Margrethe H. ; Gopal, Shuba ; Nahum, Laila A. ; Liang, Ping ; Gaasterland, Terry ; Riley, Monica

Background: Since the genome of Escherichia coli K-12 was initially annotated in 1997, additional functional information based on biological characterization and functions of sequence-similar proteins has become available. On the basis of this new information, an updated version of the annotated chromosome has been generated. Results: The E. coli K-12 chromosome is currently represented by 4,401 genes encoding 116 RNAs and 4,285 proteins. The boundaries of the genes identified in the GenBank Accession U00096 were used. Some protein-coding sequences are compound and encode multimodular proteins. The coding sequences (CDSs) are represented by modules (protein elements of at least 100 amino acids with biological activity and independent evolutionary history). There are 4,616 identified modules in the 4,285 proteins. Of these, 48.9% have been characterized, 29.5% have an imputed function, 2.1% have a phenotype and 19.5% have no function assignment. Only 7% of the modules appear unique to E. coli, and this number is expected to be reduced as more genome data becomes available. The imputed functions were assigned on the basis of manual evaluation of functions predicted by BLAST and DARWIN analyses and by the MAGPIE genome annotation system. Conclusions: Much knowledge has been gained about functions encoded by the E. coli K-12 genome since the 1997 annotation was published. The data presented here should be useful for analysis of E. coli gene products as well as gene products encoded by other genomes.
Escherichia coli K-12 : a cooperatively developed annotation snapshot—2005

(Oxford University Press, 2006-01-05) Riley, Monica ; Abe, Takashi ; Arnaud, Martha B. ; Berlyn, Mary K. B. ; Blattner, Frederick R. ; Chaudhuri, Roy R. ; Glasner, Jeremy D. ; Horiuchi, Takashi ; Keseler, Ingrid M. ; Kosuge, Takehide ; Mori, Hirotada ; Perna, Nicole T. ; Plunkett, Guy ; Rudd, Kenneth E. ; Serres, Margrethe H. ; Thomas, Gavin H. ; Thomson, Nicholas R. ; Wishart, David ; Wanner, Barry L.

The goal of this group project has been to coordinate and bring up-to-date information on all genes of Escherichia coli K-12. Annotation of the genome of an organism entails identification of genes, the boundaries of genes in terms of precise start and end sites, and description of the gene products. Known and predicted functions were assigned to each gene product on the basis of experimental evidence or sequence analysis. Since both kinds of evidence are constantly expanding, no annotation is complete at any moment in time. This is a snapshot analysis based on the most recent genome sequences of two E.coli K-12 bacteria. An accurate and up-to-date description of E.coli K-12 genes is of particular importance to the scientific community because experimentally determined properties of its gene products provide fundamental information for annotation of innumerable genes of other organisms. Availability of the complete genome sequence of two K-12 strains allows comparison of their genotypes and mutant status of alleles.
Conserved synteny at the protein family level reveals genes underlying Shewanella species’ cold tolerance and predicts their novel phenotypes

(Springer, 2009-10-03) Karpinets, Tatiana V. ; Obraztsova, Anna Y. ; Wang, Yanbing ; Schmoyer, Denise D. ; Kora, Guruprasad H. ; Park, Byung H. ; Serres, Margrethe H. ; Romine, Margaret F. ; Land, Miriam L. ; Kothe, Terence B. ; Fredrickson, James K. ; Nealson, Kenneth H. ; Uberbacher, Edward C.

Bacteria of the genus Shewanella can thrive in different environments and demonstrate significant variability in their metabolic and ecophysiological capabilities including cold and salt tolerance. Genomic characteristics underlying this variability across species are largely unknown. In this study, we address the problem by a comparison of the physiological, metabolic, and genomic characteristics of 19 sequenced Shewanella species. We have employed two novel approaches based on association of a phenotypic trait with the number of the trait-specific protein families (Pfam domains) and on the conservation of synteny (order in the genome) of the trait-related genes. Our first approach is top-down and involves experimental evaluation and quantification of the species’ cold tolerance followed by identification of the correlated Pfam domains and genes with a conserved synteny. The second, a bottom-up approach, predicts novel phenotypes of the species by calculating profiles of each Pfam domain among their genomes and following pair-wise correlation of the profiles and their network clustering. Using the first approach, we find a link between cold and salt tolerance of the species and the presence in the genome of a Na+/H+ antiporter gene cluster. Other cold-tolerance-related genes include peptidases, chemotaxis sensory transducer proteins, a cysteine exporter, and helicases. Using the bottom-up approach, we found several novel phenotypes in the newly sequenced Shewanella species, including degradation of aromatic compounds by an aerobic hybrid pathway in Shewanella woodyi, degradation of ethanolamine by Shewanella benthica, and propanediol degradation by Shewanella putrefaciens CN32 and Shewanella sp. W3-18-1.
Comparisons of Shewanella strains based on genome annotations, modeling, and experiments

(BioMed Central, 2014-03-12) Ong, Wai Kit ; Vu, Trang T. ; Lovendahl, Klaus N. ; Llull, Jenna M. ; Serres, Margrethe H. ; Romine, Margaret F. ; Reed, Jennifer L.

Shewanella is a genus of facultatively anaerobic, Gram-negative bacteria that have highly adaptable metabolism which allows them to thrive in diverse environments. This quality makes them an attractive bacterial target for research in bioremediation and microbial fuel cell applications. Constraint-based modeling is a useful tool for helping researchers gain insights into the metabolic capabilities of these bacteria. However, Shewanella oneidensis MR-1 is the only strain with a genome-scale metabolic model constructed out of 21 sequenced Shewanella strains. In this work, we updated the model for Shewanella oneidensis MR-1 and constructed metabolic models for three other strains, namely Shewanella sp. MR-4, Shewanella sp. W3-18-1, and Shewanella denitrificans OS217 which span the genus based on the number of genes lost in comparison to MR-1. We also constructed a Shewanella core model that contains the genes shared by all 21 sequenced strains and a few non-conserved genes associated with essential reactions. Model comparisons between the five constructed models were done at two levels – for wildtype strains under different growth conditions and for knockout mutants under the same growth condition. In the first level, growth/no-growth phenotypes were predicted by the models on various carbon sources and electron acceptors. Cluster analysis of these results revealed that the MR-1 model is most similar to the W3-18-1 model, followed by the MR-4 and OS217 models when considering predicted growth phenotypes. However, a cluster analysis done based on metabolic gene content revealed that the MR-4 and W3-18-1 models are the most similar, with the MR-1 and OS217 models being more distinct from these latter two strains. As a second level of comparison, we identified differences in reaction and gene content which give rise to different functional predictions of single and double gene knockout mutants using Comparison of Networks by Gene Alignment (CONGA). Here, we showed how CONGA can be used to find biomass, metabolic, and genetic differences between models. We developed four strain-specific models and a general core model that can be used to do various in silico studies of Shewanella metabolism. The developed models provide a platform for a systematic investigation of Shewanella metabolism to aid researchers using Shewanella in various biotechnology applications.
Detection of transcriptional triggers in the dynamics of microbial growth: application to the respiratorily versatile bacterium Shewanella oneidensis

(Oxford University Press, 2012-05-25) Beg, Qasim K. ; Zampieri, Mattia ; Klitgord, Niels ; Collins, Sara B. ; Altafini, Claudio ; Serres, Margrethe H. ; Segre, Daniel

The capacity of microorganisms to respond to variable external conditions requires a coordination of environment-sensing mechanisms and decision-making regulatory circuits. Here, we seek to understand the interplay between these two processes by combining high-throughput measurement of time-dependent mRNA profiles with a novel computational approach that searches for key genetic triggers of transcriptional changes. Our approach helped us understand the regulatory strategies of a respiratorily versatile bacterium with promising bioenergy and bioremediation applications, Shewanella oneidensis, in minimal and rich media. By comparing expression profiles across these two conditions, we unveiled components of the transcriptional program that depend mainly on the growth phase. Conversely, by integrating our time-dependent data with a previously available large compendium of static perturbation responses, we identified transcriptional changes that cannot be explained solely by internal network dynamics, but are rather triggered by specific genes acting as key mediators of an environment-dependent response. These transcriptional triggers include known and novel regulators that respond to carbon, nitrogen and oxygen limitation. Our analysis suggests a sequence of physiological responses, including a coupling between nitrogen depletion and glycogen storage, partially recapitulated through dynamic flux balance analysis, and experimentally confirmed by metabolite measurements. Our approach is broadly applicable to other systems.
Microbial eukaryotic predation pressure and biomass at deep-sea hydrothermal vents

(Oxford University Press, 2024-01-13) Hu, Sarah K. ; Anderson, Rika E. ; Pachiadaki, Maria G. ; Edgcomb, Virginia P. ; Serres, Margrethe H. ; Sylva, Sean P. ; German, Christopher R. ; Seewald, Jeffrey S. ; Lang, Susan Q. ; Huber, Julie A.

Deep-sea hydrothermal vent geochemistry shapes the foundation of the microbial food web by fueling chemolithoautotrophic microbial activity. Microbial eukaryotes (or protists) play a critical role in hydrothermal vent food webs as consumers and hosts of symbiotic bacteria, and as a nutritional source to higher trophic levels. We measured microbial eukaryotic cell abundance and predation pressure in low-temperature diffuse hydrothermal fluids at the Von Damm and Piccard vent fields along the Mid-Cayman Rise in the Western Caribbean Sea. We present findings from experiments performed under in situ pressure that show cell abundances and grazing rates higher than those done at 1 atmosphere (shipboard ambient pressure); this trend was attributed to the impact of depressurization on cell integrity. A relationship between the protistan grazing rate, prey cell abundance, and temperature of end-member hydrothermal vent fluid was observed at both vent fields, regardless of experimental approach. Our results show substantial protistan biomass at hydrothermally fueled microbial food webs, and when coupled with improved grazing estimates, suggest an important contribution of grazers to the local carbon export and supply of nutrient resources to the deep ocean.
Draft genome sequence of Methanocalculus natronophilus sp. Strain Z-7105T, an alkaliphilic, methanogenic archaeon isolated from a soda lake

(American Society for Microbiology, 2024-06-04) Elkassas, Sabrina M. ; Serres, Margrethe H. ; Richardson, Derrick ; Zhilina, Tatyana N. ; Huber, Julie A.

A methanogenic archaeon was isolated from bottom sediments in the vicinity of Lake Tanatar II (Altai, Russia), an alkaline soda lake. Here we present the draft genome sequence of Methanocalculus natronophilus sp. strain Z-7105T.

Serres Margrethe H.

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