Abiotic selection of microbial genome size in the global ocean

Ngugi, David K.; Acinas, Silvia G.; Sánchez, Pablo; Gasol, Josep M.; Agusti, Susana; Karl, David M.; Duarte, Carlos M.

doi:10.1038/s41467-023-36988-x

Title: Abiotic selection of microbial genome size in the global ocean

Journal Article · 13 March 2023 · Nature Communications

DOI: https://doi.org/10.1038/s41467-023-36988-x · OSTI ID:1961234

^[1];

^[2];

^[3];

^[4];

^[3]

Leibniz Institute DSMZ - German Collection of Microorganisms and Cell Cultures, Braunschweig (Germany)
Institut de Ciencies del Mar (CSIC), Barcelona (Spain)
King Abdullah University of Science and Technology (KAUST), Thuwal (Saudi Arabia)
University of Hawaii at Manoa, Honolulu, HI (United States)

Strong purifying selection is considered a major evolutionary force behind small microbial genomes in the resource-poor photic ocean. However, very little is currently known about how the size of prokaryotic genomes evolves in the global ocean and whether patterns reflect shifts in resource availability in the epipelagic and relatively stable deep-sea environmental conditions. Using 364 marine microbial metagenomes, we investigate how the average genome size of uncultured planktonic prokaryotes varies across the tropical and polar oceans to the hadal realm. We find that genome size is highest in the perennially cold polar ocean, reflecting elongation of coding genes and gene dosage effects due to duplications in the interior ocean microbiome. Moreover, the rate of change in genome size due to temperature is 16-fold higher than with depth up to 200 m. Our results demonstrate how environmental factors can influence marine microbial genome size selection and ecological strategies of the microbiome.

View Journal Article

Cite

Export

Save

Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USDOE

Grant/Contract Number:: AC02-05CH11231; AC02 05CH11231

OSTI ID:: 1961234

Alternate ID(s):: OSTI ID: 2422800

Journal Information:: Nature Communications, Vol. 14, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Environmental drivers of a microbial genomic transition zone in the ocean’s interior Mende, Daniel R.; Bryant, Jessica A.; Aylward, Frank O. Nature Microbiology, Vol. 2, Issue 10 https://doi.org/10.1038/s41564-017-0008-3	journal	August 2017
Structure and function of the Arctic and Antarctic marine microbiota as revealed by metagenomics Cao, Shunan; Zhang, Weipeng; Ding, Wei Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00826-9	journal	April 2020
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
Microbial growth in the polar oceans — role of temperature and potential impact of climate change Kirchman, David L.; Morán, Xosé Anxelu G.; Ducklow, Hugh Nature Reviews Microbiology, Vol. 7, Issue 6 https://doi.org/10.1038/nrmicro2115	journal	May 2009
Sunlight-induced DNA Damage in Marine Micro-organisms Collected Along a Latitudinal Gradient from 70°N to 68°S Meador, Jarah A.; Baldwin, Amy J.; Catala, Phillipe Photochemistry and Photobiology, Vol. 85, Issue 1 https://doi.org/10.1111/j.1751-1097.2008.00509.x	journal	January 2009
The consequences of genetic drift for bacterial genome complexity Kuo, C. -H.; Moran, N. A.; Ochman, H. Genome Research, Vol. 19, Issue 8 https://doi.org/10.1101/gr.091785.109	journal	June 2009
Deep pelagic biology Robison, Bruce H. Journal of Experimental Marine Biology and Ecology, Vol. 300, Issue 1-2 https://doi.org/10.1016/j.jembe.2004.01.012	journal	March 2004
Microbial oceanography of the dark ocean's pelagic realm Arístegui, Javier; Gasol, Josep M.; Duarte, Carlos M. Limnology and Oceanography, Vol. 54, Issue 5 https://doi.org/10.4319/lo.2009.54.5.1501	journal	June 2009
ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
Decadal trends in Red Sea maximum surface temperature Chaidez, V.; Dreano, D.; Agusti, S. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-08146-z	journal	August 2017
A Cold Limit to Adaptation in the Sea Peck, Lloyd S. Trends in Ecology & Evolution, Vol. 31, Issue 1 https://doi.org/10.1016/j.tree.2015.09.014	journal	January 2016
Compendium of 530 metagenome-assembled bacterial and archaeal genomes from the polar Arctic Ocean Royo-Llonch, Marta; Sánchez, Pablo; Ruiz-González, Clara Nature Microbiology, Vol. 6, Issue 12 https://doi.org/10.1038/s41564-021-00979-9	journal	November 2021
Seafaring in the 21St Century: The Malaspina 2010 Circumnavigation Expedition Duarte, Carlos M. Limnology and Oceanography Bulletin, Vol. 24, Issue 1 https://doi.org/10.1002/lob.10008	journal	January 2015
Deep ocean metagenomes provide insight into the metabolic architecture of bathypelagic microbial communities Acinas, Silvia G.; Sánchez, Pablo; Salazar, Guillem Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02112-2	journal	May 2021
Prochlorococcus have low global mutation rate and small effective population size Chen, Zhuoyu; Wang, Xiaojun; Song, Yu Nature Ecology & Evolution, Vol. 6, Issue 2 https://doi.org/10.1038/s41559-021-01591-0	journal	December 2021
Global Dispersal of Free-Living Microbial Eukaryote Species Finlay, B. J. Science, Vol. 296, Issue 5570 https://doi.org/10.1126/science.1070710	journal	May 2002
Effect of Temperature on In Vivo Protein Synthetic Capacity in Escherichia coli Farewell, Anne; Neidhardt, Frederick C. Journal of Bacteriology, Vol. 180, Issue 17 https://doi.org/10.1128/JB.180.17.4704-4710.1998	journal	September 1998
Accelerated evolution associated with genome reduction in a free-living prokaryote Dufresne, Alexis; Garczarek, Laurence; Partensky, Frédéric Genome Biology, Vol. 6, Issue 2, p. R14 https://doi.org/10.1186/gb-2005-6-2-r14	journal	January 2005
Genomic Islands and the Ecology and Evolution of Prochlorococcus Coleman, M. L. Science, Vol. 311, Issue 5768 https://doi.org/10.1126/science.1122050	journal	March 2006
Streamlining and Simplification of Microbial Genome Architecture Lynch, Michael Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.60.080805.142300	journal	October 2006
Novel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms Zhong, Haohui; Lehtovirta-Morley, Laura; Liu, Jiwen Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00849-2	journal	June 2020
Microbial Ecology of the Dark Ocean above, at, and below the Seafloor Orcutt, B. N.; Sylvan, J. B.; Knab, N. J. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 2 https://doi.org/10.1128/MMBR.00039-10	journal	June 2011
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Mechanisms driving genome reduction of a novel Roseobacter lineage Feng, Xiaoyuan; Chu, Xiao; Qian, Yang The ISME Journal, Vol. 15, Issue 12 https://doi.org/10.1038/s41396-021-01036-3	journal	June 2021
Sensing temperature Sengupta, Piali; Garrity, Paul Current Biology, Vol. 23, Issue 8 https://doi.org/10.1016/j.cub.2013.03.009	journal	April 2013
Mutation accumulation under UV radiation in Escherichia coli Shibai, Atsushi; Takahashi, Yusuke; Ishizawa, Yuka Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-15008-1	journal	November 2017
Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world Koonin, E. V.; Wolf, Y. I. Nucleic Acids Research, Vol. 36, Issue 21 https://doi.org/10.1093/nar/gkn668	journal	October 2008
Complete-fosmid and fosmid-end sequences reveal frequent horizontal gene transfers in marine uncultured planktonic archaea Brochier-Armanet, Céline; Deschamps, Philippe; López-García, Purificación The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.16	journal	February 2011
Reductive genome evolution at both ends of the bacterial population size spectrum Batut, Bérénice; Knibbe, Carole; Marais, Gabriel Nature Reviews Microbiology, Vol. 12, Issue 12 https://doi.org/10.1038/nrmicro3331	journal	September 2014
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Assessment of the bimodality in the distribution of bacterial genome sizes Gweon, Hyun S.; Bailey, Mark J.; Read, Daniel S. The ISME Journal, Vol. 11, Issue 3 https://doi.org/10.1038/ismej.2016.142	journal	November 2016
Temperature dependency of metabolic rates in the upper ocean: A positive feedback to global climate change? Boscolo-Galazzo, F.; Crichton, K. A.; Barker, S. Global and Planetary Change, Vol. 170 https://doi.org/10.1016/j.gloplacha.2018.08.017	journal	November 2018
Marine Bacterial Isolates Display Diverse Responses to UV-B Radiation Joux, Fabien; Jeffrey, Wade H.; Lebaron, Philippe Applied and Environmental Microbiology, Vol. 65, Issue 9 https://doi.org/10.1128/AEM.65.9.3820-3827.1999	journal	September 1999
Microeconomic principles explain an optimal genome size in bacteria Ranea, Juan A. G.; Grant, Alastair; Thornton, Janet M. Trends in Genetics, Vol. 21, Issue 1 https://doi.org/10.1016/j.tig.2004.11.014	journal	January 2005
Seasonality in Ocean Microbial Communities Giovannoni, S. J.; Vergin, K. L. Science, Vol. 335, Issue 6069 https://doi.org/10.1126/science.1198078	journal	February 2012
How Many Species Are There on Earth and in the Ocean? Mora, Camilo; Tittensor, Derek P.; Adl, Sina PLoS Biology, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pbio.1001127	journal	August 2011
Gene duplication as a mechanism of genomic adaptation to a changing environment Kondrashov, Fyodor A. Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1749 https://doi.org/10.1098/rspb.2012.1108	journal	October 2012
High proportions of bacteria and archaea across most biomes remain uncultured Steen, Andrew D.; Crits-Christoph, Alexander; Carini, Paul The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0484-y	journal	August 2019
Distinct Gene Number-Genome Size Relationships for Eukaryotes and Non-Eukaryotes: Gene Content Estimation for Dinoflagellate Genomes Hou, Yubo; Lin, Senjie PLoS ONE, Vol. 4, Issue 9 https://doi.org/10.1371/journal.pone.0006978	journal	September 2009
Resource conservation manifests in the genetic code Shenhav, Liat; Zeevi, David Science, Vol. 370, Issue 6517 https://doi.org/10.1126/science.aaz9642	journal	November 2020
A Genomic Perspective Across Earth’s Microbiomes Reveals That Genome Size in Archaea and Bacteria Is Linked to Ecosystem Type and Trophic Strategy Rodríguez-Gijón, Alejandro; Nuy, Julia K.; Mehrshad, Maliheh Frontiers in Microbiology, Vol. 12 https://doi.org/10.3389/fmicb.2021.761869	journal	January 2022
Growth Temperature and Genome Size in Bacteria Are Negatively Correlated, Suggesting Genomic Streamlining During Thermal Adaptation Sabath, Niv; Ferrada, Evandro; Barve, Aditya Genome Biology and Evolution, Vol. 5, Issue 5 https://doi.org/10.1093/gbe/evt050	journal	April 2013
Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench Liu, Jiwen; Zheng, Yanfen; Lin, Heyu Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0652-3	journal	April 2019
Temperature dependence of spontaneous mutation rates Waldvogel, Ann-Marie; Pfenninger, Markus Genome Research, Vol. 31, Issue 9 https://doi.org/10.1101/gr.275168.120	journal	July 2021
Estimators of Relative Importance in Linear Regression Based on Variance Decomposition Grömping, Ulrike The American Statistician, Vol. 61, Issue 2 https://doi.org/10.1198/000313007X188252	journal	May 2007
Combined Analyses of the ITS Loci and the Corresponding 16S rRNA Genes Reveal High Micro- and Macrodiversity of SAR11 Populations in the Red Sea Ngugi, David Kamanda; Stingl, Ulrich PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0050274	journal	November 2012
Average genome size estimation improves comparative metagenomics and sheds light on the functional ecology of the human microbiome Nayfach, Stephen; Pollard, Katherine S. Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0611-7	journal	March 2015
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00867-0	journal	June 2020
Structure and function of the global ocean microbiome Sunagawa, S.; Coelho, L. P.; Chaffron, S. Science, Vol. 348, Issue 6237 https://doi.org/10.1126/science.1261359	journal	May 2015
Streamlining and Core Genome Conservation among Highly Divergent Members of the SAR11 Clade Grote, Jana; Thrash, J. Cameron; Huggett, Megan J. mBio, Vol. 3, Issue 5 https://doi.org/10.1128/mBio.00252-12	journal	September 2012
Prokaryotic Genome Expansion Is Facilitated by Phages and Plasmids but Impaired by CRISPR Gao, Na L.; Chen, Jingchao; Wang, Teng Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02254	journal	October 2019
A general theory for temperature dependence in biology Arroyo, José Ignacio; Díez, Beatriz; Kempes, Christopher P. Proceedings of the National Academy of Sciences, Vol. 119, Issue 30 https://doi.org/10.1073/pnas.2119872119	journal	July 2022
Global diversity and biogeography of deep-sea pelagic prokaryotes Salazar, Guillem; Cornejo-Castillo, Francisco M.; Benítez-Barrios, Verónica The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.137	journal	August 2015
The significance of nitrogen cost minimization in proteomes of marine microorganisms Grzymski, Joseph J.; Dussaq, Alex M. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.72	journal	June 2011
Increased Mutation Rate Is Linked to Genome Reduction in Prokaryotes Bourguignon, Thomas; Kinjo, Yukihiro; Villa-Martín, Paula Current Biology, Vol. 30, Issue 19 https://doi.org/10.1016/j.cub.2020.07.034	journal	October 2020
Trends between gene content and genome size in prokaryotic species with larger genomes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 101, Issue 9 https://doi.org/10.1073/pnas.0308653100	journal	February 2004
Large-scale ocean connectivity and planktonic body size Villarino, Ernesto; Watson, James R.; Jönsson, Bror Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02535-8	journal	January 2018
Accelerating pathway evolution by increasing the gene dosage of chromosomal segments Tumen-Velasquez, Melissa; Johnson, Christopher W.; Ahmed, Alaa Proceedings of the National Academy of Sciences, Vol. 115, Issue 27 https://doi.org/10.1073/pnas.1803745115	journal	June 2018
Comparative Metagenomic Analysis of a Microbial Community Residing at a Depth of 4,000 Meters at Station ALOHA in the North Pacific Subtropical Gyre Konstantinidis, K. T.; Braff, J.; Karl, D. M. Applied and Environmental Microbiology, Vol. 75, Issue 16 https://doi.org/10.1128/AEM.00473-09	journal	June 2009
Theory of prokaryotic genome evolution Sela, Itamar; Wolf, Yuri I.; Koonin, Eugene V. Proceedings of the National Academy of Sciences, Vol. 113, Issue 41 https://doi.org/10.1073/pnas.1614083113	journal	October 2016
A Model of Genome Size Evolution for Prokaryotes in Stable and Fluctuating Environments Bentkowski, Piotr; Van Oosterhout, Cock; Mock, Thomas Genome Biology and Evolution, Vol. 7, Issue 8 https://doi.org/10.1093/gbe/evv148	journal	August 2015
Sequencing effort dictates gene discovery in marine microbial metagenomes Duarte, Carlos M.; Ngugi, David K.; Alam, Intikhab Environmental Microbiology, Vol. 22, Issue 11 https://doi.org/10.1111/1462-2920.15182	journal	September 2020
Scaling laws predict global microbial diversity Locey, Kenneth J.; Lennon, Jay T. Proceedings of the National Academy of Sciences, Vol. 113, Issue 21 https://doi.org/10.1073/pnas.1521291113	journal	May 2016
Genome-reconstruction for eukaryotes from complex natural microbial communities West, Patrick T.; Probst, Alexander J.; Grigoriev, Igor V. Genome Research, Vol. 28, Issue 4 https://doi.org/10.1101/gr.228429.117	journal	March 2018
Excess of non-conservative amino acid changes in marine bacterioplankton lineages with reduced genomes Luo, Haiwei; Huang, Yongjie; Stepanauskas, Ramunas Nature Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nmicrobiol.2017.91	journal	June 2017
Novel Insight into Evolutionary Process from Average Genome size in Marine Bacterioplanktonic Biota Ni, J. Applied Ecology and Environmental Research, Vol. 14, Issue 2 https://doi.org/10.15666/aeer/1402_065075	journal	January 2016
Copy number change: evolving views on gene amplification Elliott, Kathryn T.; Cuff, Laura E.; Neidle, Ellen L. Future Microbiology, Vol. 8, Issue 7 https://doi.org/10.2217/fmb.13.53	journal	July 2013
Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus Flombaum, P.; Gallegos, J. L.; Gordillo, R. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 24 https://doi.org/10.1073/pnas.1307701110	journal	May 2013
Nitrogen-fixing populations of Planctomycetes and Proteobacteria are abundant in surface ocean metagenomes Delmont, Tom O.; Quince, Christopher; Shaiber, Alon Nature Microbiology, Vol. 3, Issue 7 https://doi.org/10.1038/s41564-018-0176-9	journal	June 2018
Ohno's dilemma: Evolution of new genes under continuous selection Bergthorsson, U.; Andersson, D. I.; Roth, J. R. Proceedings of the National Academy of Sciences, Vol. 104, Issue 43 https://doi.org/10.1073/pnas.0707158104	journal	October 2007
Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean Swan, B. K.; Tupper, B.; Sczyrba, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 28 https://doi.org/10.1073/pnas.1304246110	journal	June 2013
REAT: A Regional Economic Analysis Toolbox for R Wieland, Thomas REGION, Vol. 6, Issue 3 https://doi.org/10.18335/region.v6i3.267	journal	November 2019
Following Rapoport's Rule: the geographic range and genome size of bacterial taxa decline at warmer latitudes Lear, Gavin; Lau, Kelvin; Perchec, Anne‐Marie Environmental Microbiology, Vol. 19, Issue 8 https://doi.org/10.1111/1462-2920.13797	journal	June 2017
Fast and accurate average genome size and 16S rRNA gene average copy number computation in metagenomic data Pereira-Flores, Emiliano; Glöckner, Frank Oliver; Fernandez-Guerra, Antonio BMC Bioinformatics, Vol. 20, Issue 1 https://doi.org/10.1186/s12859-019-3031-y	journal	September 2019
Temperature responses of mutation rate and mutational spectrum in an Escherichia coli strain and the correlation with metabolic rate Chu, Xiao-Lin; Zhang, Bo-Wen; Zhang, Quan-Guo BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1252-8	journal	August 2018
Metagenomic covariation along densely sampled environmental gradients in the Red Sea Thompson, Luke R.; Williams, Gareth J.; Haroon, Mohamed F. The ISME Journal, Vol. 11, Issue 1 https://doi.org/10.1038/ismej.2016.99	journal	July 2016
Insights into the Vertical Stratification of Microbial Ecological Roles across the Deepest Seawater Column on Earth Xue, Chun-Xu; Liu, Jiwen; Lea-Smith, David J. Microorganisms, Vol. 8, Issue 9 https://doi.org/10.3390/microorganisms8091309	journal	August 2020
Fast and accurate average genome size and 16S rRNA gene average copy number computation in metagenomic data Pereira-Flores, Emiliano; Glöckner, Frank; Fernandez-Guerra, Antonio figshare https://doi.org/10.6084/m9.figshare.c.4655912.v1	collection	January 2019
VIBRANT: automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences Kieft, Kristopher; Zhou, Zhichao; Anantharaman, Karthik figshare https://doi.org/10.6084/m9.figshare.c.5016656.v1	collection	January 2020

Similar Records

Metagenome-assembled genomes of phytoplankton microbiomes from the Arctic and Atlantic Oceans

Journal Article · 2022 · Microbiome · OSTI ID:1865498

Duncan, Anthony; Barry, Kerrie; Daum, Chris; +11 more

Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

Journal Article · 2022 · Microbiome · OSTI ID:1888832

Keller-Costa, Tina; Kozma, Lydia; Silva, Sandra G.; +6 more

Assembling the Marine Metagenome, One Cell at a Time

Journal Article · 2010 · PLoS One · OSTI ID:985325

Woyke, Tanja; Xie, Gary; Copeland, Alex; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Science & Technology - Other Topics
Metagenomics
Microbial ecology
Molecular ecology

Title: Abiotic selection of microbial genome size in the global ocean

Citation Formats

References (79)

Similar Records

Related Subjects