Functional metagenomic profiling of nine biomes

Department of Biology, San Diego State University, San Diego, California 92182, USA.
Nature (Impact Factor: 41.46). 11/2008; 455(7214):830. DOI: 10.1038/nature07346
Source: PubMed


Microbial activities shape the biogeochemistry of the planet and macroorganism health. Determining the metabolic processes performed by microbes is important both for understanding and for manipulating ecosystems (for example, disruption of key processes that lead to disease, conservation of environmental services, and so on). Describing microbial function is hampered by the inability to culture most microbes and by high levels of genomic plasticity. Metagenomic approaches analyse microbial communities to determine the metabolic processes that are important for growth and survival in any given environment. Here we conduct a metagenomic comparison of almost 15 million sequences from 45 distinct microbiomes and, for the first time, 42 distinct viromes and show that there are strongly discriminatory metabolic profiles across environments. Most of the functional diversity was maintained in all of the communities, but the relative occurrence of metabolisms varied, and the differences between metagenomes predicted the biogeochemical conditions of each environment. The magnitude of the microbial metabolic capabilities encoded by the viromes was extensive, suggesting that they serve as a repository for storing and sharing genes among their microbial hosts and influence global evolutionary and metabolic processes.

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Available from: Brandon K. Swan, Oct 04, 2015
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    • "We also observed an enrichment of reads matching cofactors, vitamins, prosthetic groups and pigments in the viral fraction (Figure 3A), which falls in line with studies identifying these types of genes on cyanophage genomes. Genes encoding vitamin B12 [53], [54], and the pigments psbA/D [55]–[58] and pebS [23] have previously been identified on cyanophage genomes. These virally encoded genes are thought to supplement host metabolism during infection, and similar processes may occur in this vent ecosystem. "
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    ABSTRACT: The deep-sea hydrothermal vent habitat hosts a diverse community of archaea and bacteria that withstand extreme fluctuations in environmental conditions. Abundant viruses in these systems, a high proportion of which are lysogenic, must also withstand these environmental extremes. Here, we explore the evolutionary strategies of both microorganisms and viruses in hydrothermal systems through comparative analysis of a cellular and viral metagenome, collected by size fractionation of high temperature fluids from a diffuse flow hydrothermal vent. We detected a high enrichment of mobile elements and proviruses in the cellular fraction relative to microorganisms in other environments. We observed a relatively high abundance of genes related to energy metabolism as well as cofactors and vitamins in the viral fraction compared to the cellular fraction, which suggest encoding of auxiliary metabolic genes on viral genomes. Moreover, the observation of stronger purifying selection in the viral versus cellular gene pool suggests viral strategies that promote prolonged host integration. Our results demonstrate that there is great potential for hydrothermal vent viruses to integrate into hosts, facilitate horizontal gene transfer, and express or transfer genes that manipulate the hosts' functional capabilities.
    PLoS ONE 10/2014; 9(10):e109696. DOI:10.1371/journal.pone.0109696 · 3.23 Impact Factor
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    • "The vast sequence diversity in environmental metagenomes suggests a similar magnitude of metabolic and biochemical diversity (Dinsdale et al. 2008; Yooseph et al. 2007), but the latter is impossible to comprehensively describe based only on sequence analysis due to the presence of the large number of unknown or poorly characterized genes. This necessitates the development of experimental approaches for metagenome research including new cultivation technologies, meta-transcriptomics, meta-proteomics and activity-based screening methods (Ferrer et al. 2007; Giovannoni and Stingl 2007; Ram et al. 2005; Simon and Daniel 2011; Uchiyama and Miyazaki 2009). "
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    ABSTRACT: Most of the Earth's biosphere is cold and is populated by cold-adapted microorganisms. To explore the natural enzyme diversity of these environments and identify new carboxylesterases, we have screened three marine metagenome gene libraries for esterase activity. The screens identified 23 unique active clones, from which five highly active esterases were selected for biochemical characterization. The purified metagenomic esterases exhibited high activity against α-naphthyl and p-nitrophenyl esters with different chain lengths. All five esterases retained high activity at 5 °C indicating that they are cold-adapted enzymes. The activity of MGS0010 increased more than two times in the presence of up to 3.5 M NaCl or KCl, whereas the other four metagenomic esterases were inhibited to various degrees by these salts. The purified enzymes showed different sensitivities to inhibition by solvents and detergents, and the activities of MGS0010, MGS0105 and MGS0109 were stimulated three to five times by the addition of glycerol. Screening of purified esterases against 89 monoester substrates revealed broad substrate profiles with a preference for different esters. The metagenomic esterases also hydrolyzed several polyester substrates including polylactic acid suggesting that they can be used for polyester depolymerization. Thus, esterases from marine metagenomes are cold-adapted enzymes exhibiting broad biochemical diversity reflecting the environmental conditions where they evolved.
    Applied Microbiology and Biotechnology 09/2014; 99(5). DOI:10.1007/s00253-014-6038-3 · 3.34 Impact Factor
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    • "If we assume that a single genome encodes 4000 proteins (as is the case for the typical bacteria Escherichia coli), then 4 × 10 8 potential proteins might be expected in just 1 g of soil. Supposing that 40% of these proteins display catalytic activity (Dinsdale et al., 2008), we might expect to find 1.6 × 10 8 biocatalysts, which highlights the vast inventory of biological functions available in nature. Metagenomics avoids the necessity of isolation and laboratory cultivation of individual microorganisms, and has become a powerful tool for accessing and exploring the biological and molecular biodiversity present in different natural environments . "
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    ABSTRACT: There is a growing demand for enzymes with improved catalytic performance or tolerance to process-specific parameters, and biotechnology plays a crucial role in the development of biocatalysts for use in industry, agriculture, medicine and energy generation. Metagenomics takes advantage of the wealth of genetic and biochemical diversity present in the genomes of microorganisms found in environmental samples, and provides a set of new technologies directed towards screening for new catalytic activities from environmental samples with potential biotechnology applications. However, biased and low level of expression of heterologous proteins in Escherichia coli together with the use of non-optimal cloning vectors for the construction of metagenomic libraries generally results in an extremely low success rate for enzyme identification. The bottleneck arising from inefficient screening of enzymatic activities has been addressed from several perspectives; however, the limitations related to biased expression in heterologous hosts cannot be overcome by using a single approach, but rather requires the synergetic implementation of multiple methodologies. Here, we review some of the principal constraints regarding the discovery of new enzymes in metagenomic libraries and discuss how these might be resolved by using synthetic biology methods.
    Microbial Biotechnology 09/2014; 8(1). DOI:10.1111/1751-7915.12146 · 3.21 Impact Factor
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