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Increased Mutation Rate is Linked to Genome Reduction in Prokaryotes

32 Pages Posted: 10 Feb 2020 Publication Status: Review Complete

See all articles by Thomas Bourguignon

Thomas Bourguignon

Okinawa Institute of Science and Technology Graduate University (OIST)

Yukihiro Kinjo

Okinawa Institute of Science and Technology Graduate University (OIST)

Paula Villa-Martin

Okinawa Institute of Science and Technology Graduate University (OIST)

Nicholas V. Coleman

The University of Sydney - School of Life and Environmental Sciences

Qian Tang

National University of Singapore (NUS) - Department of Biological Sciences

Daej A. Arab

The University of Sydney - School of Life and Environmental Sciences

Zongqing Wang

Southwest University - College of Plant Protection

Gaku Tokuda

University of the Ryukyus - Tropical Biosphere Research Center

Yuichi Hongoh

Tokyo Institute of Technology - School of Life Science and Technology

Moriya Ohkuma

RIKEN Bioresource Research Centre

Simon Y. W. Ho

The University of Sydney - School of Life and Environmental Sciences

Simone Pigolotti

Okinawa Institute of Science and Technology Graduate University (OIST)

Nathan Lo

The University of Sydney - School of Life and Environmental Sciences

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Abstract

The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size, a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission. However, the existence of reduced genomes in marine and terrestrial prokaryote species with large Ne demand an alternative explanation. One such alternative is enhanced mutation rate, which might increase an organism’s ability to adapt to novel environments, but might also promote gene loss. We employed a novel approach involving molecular evolutionary and phylogenomic analyses of nine lineages of prokaryotes that display various levels of genome reduction: Blattabacterium and Buchnera insect endosymbionts, marine Prochlorococcus and Synechococcus, the thermophilic archaean Thermococcus, and five lineages of free-living bacteria belonging to the Proteobacteria, Actinobacteria, and Bacteroidetes. We found that rates of gene loss strongly correlate with mutation rates in all of these groups, with the exception of two lineages of free-living bacteria, and show weak or no correlation with the ratio of nonsynonymous/synonymous substitution rates (dN/dS). This indicates that genome reduction is largely associated with increased mutation rate, while the association between gene loss and changes in Ne is less well defined. Lineages with relatively high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar underlying mechanisms drive genome reduction in both intracellular and free-living prokaryotes, with implications for developing a comprehensive theory of prokaryote genome size evolution.

Keywords: endosymbionts, genome evolution, phylogenetic tree, population size

Suggested Citation

Bourguignon, Thomas and Kinjo, Yukihiro and Villa-Martin, Paula and Coleman, Nicholas V. and Tang, Qian and Arab, Daej A. and Wang, Zongqing and Tokuda, Gaku and Hongoh, Yuichi and Ohkuma, Moriya and Ho, Simon Y. W. and Pigolotti, Simone and Lo, Nathan, Increased Mutation Rate is Linked to Genome Reduction in Prokaryotes. Available at SSRN: https://ssrn.com/abstract=3532768 or http://dx.doi.org/10.2139/ssrn.3532768
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Thomas Bourguignon (Contact Author)

Okinawa Institute of Science and Technology Graduate University (OIST) ( email )

1919-1 Tancha, Onna-son, Kunigami-gun
Okinawa, 904-0495
Japan

Yukihiro Kinjo

Okinawa Institute of Science and Technology Graduate University (OIST)

1919-1 Tancha, Onna-son, Kunigami-gun
Okinawa, 904-0495
Japan

Paula Villa-Martin

Okinawa Institute of Science and Technology Graduate University (OIST)

1919-1 Tancha, Onna-son, Kunigami-gun
Okinawa, 904-0495
Japan

Nicholas V. Coleman

The University of Sydney - School of Life and Environmental Sciences

Level 5, Carslaw Building (F07)
Sydney, New South Wales 2006
Australia

Qian Tang

National University of Singapore (NUS) - Department of Biological Sciences

14 Science Drive 4
Singapore, 117543
China

Daej A. Arab

The University of Sydney - School of Life and Environmental Sciences

Level 5, Carslaw Building (F07)
Sydney, New South Wales 2006
Australia

Zongqing Wang

Southwest University - College of Plant Protection

China

Gaku Tokuda

University of the Ryukyus - Tropical Biosphere Research Center

Japan

Yuichi Hongoh

Tokyo Institute of Technology - School of Life Science and Technology

2-12-1 O-okayama, Meguro-ku
Tokyo 152-8550, 52-8552
Japan

Moriya Ohkuma

RIKEN Bioresource Research Centre

Japan

Simon Y. W. Ho

The University of Sydney - School of Life and Environmental Sciences

Level 5, Carslaw Building (F07)
Sydney, New South Wales 2006
Australia

Simone Pigolotti

Okinawa Institute of Science and Technology Graduate University (OIST)

1919-1 Tancha, Onna-son, Kunigami-gun
Okinawa, 904-0495
Japan

Nathan Lo

The University of Sydney - School of Life and Environmental Sciences

Level 5, Carslaw Building (F07)
Sydney, New South Wales 2006
Australia

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