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High transcriptional activity of insertion sequences in Baltic Sea microorganisms
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Insertion sequences (ISs) are mobile genetic elements found in almost all prokaryotic genomes. They consist of a gene encoding a transposase, surrounded by inverted repeats. The transposase has the ability to excise the IS and insert it elsewhere in the genome, a process referred to as transposition. ISs have high copy numbers in prokaryotes inhabiting “extreme” environments, and it is proposed that their activity facilitates adaptation to environmental changes and subsequent adaptive evolution. The initial step in the transposition of an IS is the transcription of the open reading frame encoding the transposase. In an effort to evaluate the presence, activity and role of ISs in microbes of a temperate water body offering steep changes in salinity and nutrient conditions, the metatranscriptomes and metagenomes of ten water samples from the brackish water Baltic Sea were examined. ISs in the limnic Lake Torne Träsk, the marine waters off the Swedish west coast and off the coast of California were included to get perspective. The results reveal that insertion sequences make up a considerably higher fraction of the metatranscriptomes of brackish waters (0.3-1.8%) than of marine waters (0.0005-0.2%), and that the IS fraction of the metatranscriptome is commonly double that of the IS fraction of the metagenome. From these data it is concluded that ISs occupy a significant part of Baltic Sea bacterial transcription activity, in line with their proposed function as facilitators of adaptive change to changing and stressful environments.

National Category
Microbiology
Research subject
Plant Physiology
Identifiers
URN: urn:nbn:se:su:diva-117088OAI: oai:DiVA.org:su-117088DiVA: diva2:810169
Available from: 2015-05-06 Created: 2015-05-06 Last updated: 2016-01-29Bibliographically approved
In thesis
1. Effects and Dynamics of Insertion Sequences in the Evolution of Cyanobacteria
Open this publication in new window or tab >>Effects and Dynamics of Insertion Sequences in the Evolution of Cyanobacteria
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Cyanobacteria are globally widespread and ecologically highly significant photoautotrophic microorganisms, with diverse geno- and phenotypic characters unprecedented among prokaryotes. This phylum embraces representatives with an exclusive adaptability in highly specialized environments, from oligotrophic ocean waters to the interior of cells in symbiotic plants, the most extreme being the chloroplasts. Insertion sequences (ISs) are short (~1000 bp) mobile genetic elements prevalent in microbial genomes, potentially representing potent adaptive forces.

In this thesis, hypotheses tested that ISs play significant roles in both reductive and adaptive evolution in physiologically versatile cyanobacteria, using two model systems. First, the genome of an obligate plant (Azolla) symbiont, the cyanobacterium ‘Nostoc azollae 0708’, was sequenced, which led to the discovery of a highly ‘eroding’ genome (5,48 Mbp), loaded with ISs covering 14% of the genome, a situation likely caused by the relaxed selection pressure within the plant. The ISs were located in close proximity to the extremely numerous pseudogenes identified, although genes with key functions in a symbiotic context escaped IS mediated erosion (e.g. nitrogen fixation and differentiation genes). Some ISs were shown to have transposed short distances within the genome (‘local hoping’), and to be likely causative agents in pseudogene formation, and thus pivotal actors in the reductive evolution discovered.

To widen the scope of ISs further, additionally 66 phylogenetically diverse microorganisms with a variety of life styles (free-living, symbionts, pathogens) were examined in regards to ISs influence. The data verified their over-all importance in shaping microbial genomes.

Finally, natural microbial populations in the Baltic Sea, a semi-enclosed geologically young (~10,000 years) brackish water body offering steep gradients in salinity and nutrient loads, were examined using metatranscriptomics and metagenomics. A large proportion of the metagenome was devoted to ISs and most importantly a large fraction of the metatranscriptome consisted of IS transcripts (~1%), which may be suggestive of a high IS activity. These phenomena were most apparent in cyanobacteria in central parts of the Baltic Sea. The presence of an especially rich abundance of ISs in brackish waters was further substantiated by their low frequency (< 0.1%) in microbes of marine waters. Hence, ISs may facilitate both adaptations (short term) and adaptive evolution (long term) in microbes entering brackish water, otherwise unable to cross the distinct limnic-to-marine salinity-divide. Together, the data reveal high genomic loads of ISs in cyanobacteria subject to highly demanding conditions and stress the importance of locally migrating ISs (and pseudogenization) as important facilitators in adaptation and evolution, being a more rapid process than hitherto expected. The findings strongly support current theories stating a crucial role of ISs in shaping microbial genomes to render fitness.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2015. 56 p.
Keyword
Cyanobacteria, Insertion Sequences, Evolution
National Category
Botany
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-117090 (URN)978-91-7649-191-1 (ISBN)
Public defence
2015-06-10, Lecture Hall, Department of Ecology, Environment and Plant Sciences, Lilla Frescativägen 5, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 3: Manuscript.

Available from: 2015-05-19 Created: 2015-05-06 Last updated: 2015-12-02Bibliographically approved

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