Universität zu Köln

Power, Jeffrey J., Pinheiro, Fernanda ORCID: 0000-0002-0132-0562, Pompei, Simone, Kovacova, Viera ORCID: 0000-0003-4581-4254, Yueksel, Melih, Rathmann, Isabel ORCID: 0000-0003-0596-9630, Foerster, Mona, Laessig, Michael and Maier, Berenike ORCID: 0000-0001-6971-9927 (2021). Adaptive evolution of hybrid bacteria by horizontal gene transfer. Proc. Natl. Acad. Sci. U. S. A., 118 (10). WASHINGTON: NATL ACAD SCIENCES. ISSN 0027-8424

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Abstract

Horizontal gene transfer (HGT) is an important factor in bacterial evolution that can act across species boundaries. Yet, we know little about rate and genomic targets of cross-lineage gene transfer and about its effects on the recipient organism's physiology and fitness. Here, we address these questions in a parallel evolution experiment with two Bacillus subtilis lineages of 7% sequence divergence. We observe rapid evolution of hybrid organisms: gene transfer swaps similar to 12% of the core genome in just 200 generations, and 60% of core genes are replaced in at least one population. By genomics, transcriptomics, fitness assays, and statistical modeling, we show that transfer generates adaptive evolution and functional alterations in hybrids. Specifically, our experiments reveal a strong, repeatable fitness increase of evolved populations in the stationary growth phase. By genomic analysis of the transfer statistics across replicate populations, we infer that selection on HGT has a broad genetic basis: 40% of the observed transfers are adaptive. At the level of functional gene networks, we find signatures of negative, positive, and epistatic selection, consistent with hybrid incompatibilities and adaptive evolution of network functions. Our results suggest that gene transfer navigates a complex cross-lineage fitness landscape, bridging epistatic barriers along multiple high-fitness paths.

Item Type:	Journal Article
Creators:	Creators Email ORCID ORCID Put Code Power, Jeffrey J. UNSPECIFIED UNSPECIFIED UNSPECIFIED Pinheiro, Fernanda UNSPECIFIED orcid.org/0000-0002-0132-0562 UNSPECIFIED Pompei, Simone UNSPECIFIED UNSPECIFIED UNSPECIFIED Kovacova, Viera UNSPECIFIED orcid.org/0000-0003-4581-4254 UNSPECIFIED Yueksel, Melih UNSPECIFIED UNSPECIFIED UNSPECIFIED Rathmann, Isabel UNSPECIFIED orcid.org/0000-0003-0596-9630 UNSPECIFIED Foerster, Mona UNSPECIFIED UNSPECIFIED UNSPECIFIED Laessig, Michael UNSPECIFIED UNSPECIFIED UNSPECIFIED Maier, Berenike UNSPECIFIED orcid.org/0000-0001-6971-9927 UNSPECIFIED
URN:	urn:nbn:de:hbz:38-562890
DOI:	10.1073/pnas.2007873118
Journal or Publication Title:	Proc. Natl. Acad. Sci. U. S. A.
Volume:	118
Number:	10
Date:	2021
Publisher:	NATL ACAD SCIENCES
Place of Publication:	WASHINGTON
ISSN:	0027-8424
Language:	English
Faculty:	Unspecified
Divisions:	Unspecified
Subjects:	no entry
Uncontrolled Keywords:	Keywords Language BACILLUS-SUBTILIS; NATURAL TRANSFORMATION; DNA UPTAKE; SPECIATION; BENEFITS; BARRIERS; FITNESS Multiple languages Multidisciplinary Sciences Multiple languages
URI:	http://kups.ub.uni-koeln.de/id/eprint/56289