Abstract
BackgroundNon-coding RNAs (ncRNAs), which perform diverse regulatory roles, have been found in organisms from all superkingdoms of life. However, there have been limited numbers of studies on the functions of ncRNAs, especially in nonmodel organisms such as Kluyveromyces marxianus that is widely used in the field of industrial biotechnology.ResultsIn this study, we measured changes in transcriptome at three time points during the exponential growth phase of K. marxianus by using strand-specific RNA-seq. We found that approximately 60 % of the transcriptome consists of ncRNAs transcribed from antisense and intergenic regions of the genome that were transcribed at lower levels than mRNA. In the transcriptome, a substantial number of long antisense ncRNAs (lancRNAs) are differentially expressed and enriched in carbohydrate and energy metabolism pathways. Furthermore, this enrichment is evolutionarily conserved, at least in yeast. Particularly, the mode of regulation of mRNA/lancRNA pairs is associated with mRNA transcription levels; the correlation between the pairs is positive at high mRNA transcriptional levels and negative at low levels. In addition, significant induction of mRNA and coverage of more than half of the mRNA sequence by a lancRNA strengthens the positive correlation between mRNA/lancRNA pairs.ConclusionsTranscriptome sequencing of K. marxianus in the exponential growth phase reveals pervasive transcription of ncRNAs with evolutionarily conserved functions. Studies of the mode of regulation of mRNA/lancRNA pairs suggest that induction of lancRNA may be associated with switch-like behavior of mRNA/lancRNA pairs and efficient regulation of the carbohydrate and energy metabolism pathways in the exponential growth phase of K. marxianus being used in industrial applications.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2474-z) contains supplementary material, which is available to authorized users.
Highlights
Non-coding RNAs, which perform diverse regulatory roles, have been found in organisms from all superkingdoms of life
Regulatory roles of non-coding RNA (ncRNA) In order to investigate whether pervasive ncRNA transcription at the exponential growth phase plays a functions, we focused on messenger RNA (mRNA), long antisense non-coding RNA (lancRNA), and short antisense non-coding RNA (sancRNA), as the functions of genes within these RNA classes may be inferred from gene annotation [20]
Taking all the mRNA/lancRNA pairs into account, our results showed weak positive correlation between lancRNA and mRNA which was consistent with findings in S. cerevisiae (Fig. 4a)
Summary
Non-coding RNAs (ncRNAs), which perform diverse regulatory roles, have been found in organisms from all superkingdoms of life. The haploid and thermotolerant Kluyveromyces marxianus is a non-conventional yeast species with several advantageous metabolic properties over Saccharomyces cerevisiae, such as fermentation ability at high temperatures, ability to grow on various hexose and pentose sugars, production of less ethanol in the presence of excessive sugar, and weak glucose repression, which enables the fermentation of. It has been established that transcriptional regulatory networks, comprising of transcription factors and other auxiliary components, control metabolic flexibility and robustness in response to environmental conditions. A full understanding of the cellular response to growth conditions as well as the roles of cognate regulators, such as transcription factors, is necessary for the elucidation of changes in transcript levels of metabolic genes due to the effects of growth conditions
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