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Review
. 2016 Sep 8:70:235-54.
doi: 10.1146/annurev-micro-102215-095748.

Evolution and Ecology of Actinobacteria and Their Bioenergy Applications

Affiliations
Review

Evolution and Ecology of Actinobacteria and Their Bioenergy Applications

Gina R Lewin et al. Annu Rev Microbiol. .

Abstract

The ancient phylum Actinobacteria is composed of phylogenetically and physiologically diverse bacteria that help Earth's ecosystems function. As free-living organisms and symbionts of herbivorous animals, Actinobacteria contribute to the global carbon cycle through the breakdown of plant biomass. In addition, they mediate community dynamics as producers of small molecules with diverse biological activities. Together, the evolution of high cellulolytic ability and diverse chemistry, shaped by their ecological roles in nature, make Actinobacteria a promising group for the bioenergy industry. Specifically, their enzymes can contribute to industrial-scale breakdown of cellulosic plant biomass into simple sugars that can then be converted into biofuels. Furthermore, harnessing their ability to biosynthesize a range of small molecules has potential for the production of specialty biofuels.

Keywords: Streptomyces; actinomycetes; biofuels; biotechnology; cellulases; symbiosis.

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Figures

Figure 1
Figure 1
Actinobacterial phylogenomics and relative abundance across ecosystems. Forty-six publicly available 16S rRNA gene datasets, spanning four ecosystems, were analyzed to determine the average relative percentage of reads assigned to each actinobacterial genus (93) (Supplemental Table 1; follow the Supplemental Material link from the Annual Reviews home page at http://www.annualreviews.org). Phylogenetic analysis was performed using concatenated alignments from 94 conserved TIGRFAM protein families in representative complete actinobacterial genomes (Supplemental Table 2), with the outgroup Deinococcus. Sequences were aligned with MAFFT 7.221, and the phylogeny was generated using RAxML 8.1.24 (67, 124). Molecular clock calculations were performed with RelTime using the origin of life (3,500–3,800 million years ago), the origin of Cyanobacteria (2,500–3,500 million years ago), and the Escherichia-Salmonella divergence time (50–150 million years ago) as calibration points (133). Statistical support for the phylogeny, based on a sequence resampling bootstrap analysis, is shown on nodes with less than 100% support.
Figure 2
Figure 2
Actinobacteria in nature. (a) An Acromyrmex leaf-cutter ant in her fungus garden covered in white Pseudonocardia bacteria. (b) A Streptomyces strain growing on decaying plant biomass. (c) Frankia nodules on the roots of a Russian olive tree. (d) X-ray showing a healthy lung on the left and Mycobacterium tuberculosis growth on the right. Illustrations courtesy of Gina Lewin.
Figure 3
Figure 3
Enrichment of (a) CAZy (carbohydrate-active enzyme) domains and (b) biosynthetic gene clusters in select actinobacterial genera (Supplemental Table 3). Each median value is indicated by the line within the box, each mean value is indicated by the black dot, and outliers are indicated with gray plus signs. CAZy domains were identified using the CAZy database (80). Putative biosynthetic gene clusters were identified through genome searches for conserved elements of polyketide, terpene, and nonribosomal peptide biosynthesis enzymes. Hits <30 kb apart were called the same cluster. The number of clusters may be overestimated in draft genomes.
Figure 4
Figure 4
Molecular details of the proposed role of Actinobacteria in biofuels. (a) Use of Actinobacteria for the deconstruction of plant biomass. ❶ Lytic polysaccharide monooxygenases and ❷ endoglucanases create internal cuts in the cellulose structure, creating free ends. ❸ Reducing- and nonreducing-end exoglucanases break cellulose chains into glucose and cellobiose. Additionally, ❹ peroxidases may break apart lignin, and ❺ hemicellulases hydrolyze xylan, mannan, and other hemicelluloses into constituent sugars. ❻ Cellobiose is imported into the cell, where it ❼ binds to the CebR repressor, releasing the repressor from the DNA and ❽ allowing RNA polymerase to transcribe cellulase genes. ❾ These cellulases are secreted from the cell using the Tat or Sec pathways. (b) Use of Actinobacteria for the production of biofuels. ❶ Cellobiose also is broken by β-glucosidases into glucose, which enters central metabolism. ❷ These sugars are processed in the cell and ❸ can be used for production of secreted fuel compounds, such as bisabolene, 1-propanol, or various fatty acid alkyl ester (FAAE) species where R1 is a small alkyl group and R2 is an aliphatic hydrocarbon. Currently, there are limited examples of cells that can both degrade plant biomass and produce fuel compounds, but we propose this scheme as one possible future direction in actinobacterial biofuels research.

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