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. 2020 Jul 7:11:1527.
doi: 10.3389/fmicb.2020.01527. eCollection 2020.

Comparative Genomics Discloses the Uniqueness and the Biosynthetic Potential of the Marine Cyanobacterium Hyella patelloides

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Comparative Genomics Discloses the Uniqueness and the Biosynthetic Potential of the Marine Cyanobacterium Hyella patelloides

Ângela Brito et al. Front Microbiol. .

Abstract

Baeocytous cyanobacteria (Pleurocapsales/Subsection II) can thrive in a wide range of habitats on Earth but, compared to other cyanobacterial lineages, they remain poorly studied at genomic level. In this study, we sequenced the first genome from a member of the Hyella genus - H. patelloides LEGE 07179, a recently described species isolated from the Portuguese foreshore. This genome is the largest of the thirteen baeocyte-forming cyanobacterial genomes sequenced so far, and diverges from the most closely related strains. Comparative analysis revealed strain-specific genes and horizontal gene transfer events between H. patelloides and its closest relatives. Moreover, H. patelloides genome is distinctive by the number and diversity of natural product biosynthetic gene clusters (BGCs). The majority of these clusters are strain-specific BGCs with a high probability of synthesizing novel natural products. One BGC was identified as being putatively involved in the production of terminal olefin. Our results showed that, H. patelloides produces hydrocarbon with C15 chain length, and synthesizes C14, C16, and C18 fatty acids exceeding 4% of the dry cell weight. Overall, our data contributed to increase the information on baeocytous cyanobacteria, and shed light on H. patelloides evolution, phylogeny and natural product biosynthetic potential.

Keywords: Hyella; biosynthetic gene clusters; cyanobacteria; genome; natural products.

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Figures

FIGURE 1
FIGURE 1
Light (A1,A2) and transmission electron (A3) micrographs of Hyella patelloides LEGE 07179. Geographical location (B1), graphical representation (B2) and image of the sampling site (B3). Scale bars: (A1,A2), 20 μm; (A3), 0.5 μm.
FIGURE 2
FIGURE 2
Bayesian phylogenetic tree based on 1209 concatenated orthologous genes shared between Hyella patelloides LEGE 07179 and the cyanobacterial strains selected for this analysis. Moorea producens 3L and Cyanothece sp. PCC 8802 were used to root the tree. Numbers along branches indicate posterior credibility probability values. The strains’ habitat is highlighted by different colors: Blue – marine; Green – freshwater; Brown – soil; Pink – rice field.
FIGURE 3
FIGURE 3
Comparison of the synonymous rate (Ks) distributions based on sets of 500 non-overlapping synonymous sites obtained using concatenated gene alignments. All – sets of genes for which a putative orthologous gene was found in all species; Pair – genes for which the ortholog was found only in Hyella patelloides LEGE 07179 and the analyzed strain.
FIGURE 4
FIGURE 4
Percentage of Hyella patelloides LEGE 07179 genes identified as conserved protein of unknown function/protein with recognizable function, transposase or non-conserved protein of unknown function absent in one or more of the baeocyte-forming cyanobacteria studied. Class 1 – genes absent in one strain; Class 2 – genes absent in two strains; Class 3 – genes absent in three strains; Class 4 – genes absent in four strains; Class 5 – genes absent in five strains; Class 6 – genes absent in six strains (only present in H. patelloides).
FIGURE 5
FIGURE 5
Frequency of genes from the different classes analyzed (1 to 5) per baeocyte-forming cyanobacterial strain studied. Class 1 – genes absent in one strain; Class 2 – genes absent in two strains; Class 3 – genes absent in three strains; Class 4 – genes absent in four strains; Class 5 – genes absent in five strains.
FIGURE 6
FIGURE 6
Fraction of Hyella patelloides LEGE 07179, Stanieria cyanosphaera PCC 7437 and Stanieria sp. NIES 3757 genomes constituted by plasmids, using PlasFlow with different cut-offs (number between brackets).
FIGURE 7
FIGURE 7
PKS Gene cluster shared by Hyella patelloides LEGE 07179 and Pleurocapsa sp. PCC 7319. The genes are color coded according to their putative function: green for PKS (with the domains listed), dark green for 3-oxoacyl synthase, orange for cytochrome P450, pink for NAD(P)-binding domain-containing protein, blue for sulfotransferase, red for transporter, black for methyltransferase and gray for unknown proteins. KS, ketosynthase; AT, acyltransferase; ACP, acyl carrier protein; TE, thioesterase; DH, dehydratase. Further details provided in Supplementary Table S13.
FIGURE 8
FIGURE 8
Hydrocarbon profile of Hyella patelloides LEGE 07179. Terminal olefins with chain length of C15 were identified (A), and fatty acid composition of Hyella patelloides with chain lengths of C14, C16, and C18 were identified (B). Number after the colon indicates the number of double bonds, while the number after the triangle indicates the position of the double bound. Data are the means of three biological replicates, and error bars represent standard deviations.

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