Genetic and Structural Diversity of Prokaryotic Ice-Binding Proteins from the Central Arctic Ocean.

Winder, Johanna C.; Boulton, William; Salamov, Asaf; Eggers, Sarah Lena; Metfies, Katja; Moulton, Vincent; Mock, Thomas

doi:10.3390/genes14020363

Title: Genetic and Structural Diversity of Prokaryotic Ice-Binding Proteins from the Central Arctic Ocean.

Journal Article · Mon Jan 30 00:00:00 EST 2023 · Genes

DOI:https://doi.org/10.3390/genes14020363· OSTI ID:1970326

Winder, Johanna C. ^[1]; Boulton, William ^[2]; Salamov, Asaf ^[3]; Eggers, Sarah Lena ^[4]; Metfies, Katja ^[4]; Moulton, Vincent ^[1]; Mock, Thomas ^[1]

Univ. of East Anglia, Norwich (United Kingdom)
Univ. of East Anglia, Norwich (United Kingdom); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Alfred Wegener Inst., Bremerhaven (Germany)

Ice-binding proteins (IBPs) are a group of ecologically and biotechnologically relevant enzymes produced by psychrophilic organisms. Although putative IBPs containing the domain of unknown function (DUF) 3494 have been identified in many taxa of polar microbes, our knowledge of their genetic and structural diversity in natural microbial communities is limited. Here, we used samples from sea ice and sea water collected in the central Arctic Ocean as part of the MOSAiC expedition for metagenome sequencing and the subsequent analyses of metagenome-assembled genomes (MAGs). By linking structurally diverse IBPs to particular environments and potential functions, we reveal that IBP sequences are enriched in interior ice, have diverse genomic contexts and cluster taxonomically. Their diverse protein structures may be a consequence of domain shuffling, leading to variable combinations of protein domains in IBPs and probably reflecting the functional versatility required to thrive in the extreme and variable environment of the central Arctic Ocean.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Natural Environment Research Council (NERC); United Kingdom Research and Innovation (UKRI); Research Council of Norway

Grant/Contract Number:: AC02-05CH11231; OPP-1735862; NE/S007334/1; BB/T008717/1; 280292

OSTI ID:: 1970326

Journal Information:: Genes, Vol. 14, Issue 2; ISSN 2073-4425

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (68)

DOE JGI Metagenome Workflow Clum, Alicia; Huntemann, Marcel; Bushnell, Brian mSystems, Vol. 6, Issue 3 https://doi.org/10.1128/mSystems.00804-20	journal	June 2021
An ice‐binding and tandem beta‐sandwich domain‐containing protein in Shewanella frigidimarina is a potential new type of ice adhesin Vance, Tyler D. R.; Graham, Laurie A.; Davies, Peter L. The FEBS Journal, Vol. 285, Issue 8 https://doi.org/10.1111/febs.14424	journal	December 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
A bacterial ice-binding protein from the Vostok ice core Raymond, James A.; Christner, Brent C.; Schuster, Stephan C. Extremophiles, Vol. 12, Issue 5 https://doi.org/10.1007/s00792-008-0178-2	journal	July 2008
Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus Foster, Timothy J.; Geoghegan, Joan A.; Ganesh, Vannakambadi K. Nature Reviews Microbiology, Vol. 12, Issue 1 https://doi.org/10.1038/nrmicro3161	journal	December 2013
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
New Cysteine-Rich Ice-Binding Protein Secreted from Antarctic Microalga, Chloromonas sp. Jung, Woongsic; Campbell, Robert L.; Gwak, Yunho PLOS ONE, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pone.0154056	journal	April 2016
High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms Krembs, C.; Eicken, H.; Junge, K. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 49, Issue 12 https://doi.org/10.1016/S0967-0637(02)00122-X	journal	December 2002
Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice Bayer-Giraldi, Maddalena; Weikusat, Ilka; Besir, Hüseyin Cryobiology, Vol. 63, Issue 3 https://doi.org/10.1016/j.cryobiol.2011.08.006	journal	December 2011
An intracellular antifreeze protein from an Antarctic microalga that responds to various environmental stresses Gwak, Yunho; Jung, Woongsic; Lee, Yew The FASEB Journal, Vol. 28, Issue 11 https://doi.org/10.1096/fj.14-256388	journal	August 2014
Multiomics in the central Arctic Ocean for benchmarking biodiversity change Mock, Thomas; Boulton, William; Balmonte, John-Paul PLOS Biology, Vol. 20, Issue 10 https://doi.org/10.1371/journal.pbio.3001835	journal	October 2022
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice Underwood, Gjc; Fietz, S.; Papadimitriou, S. Marine Ecology Progress Series, Vol. 404 https://doi.org/10.3354/meps08557	journal	April 2010
Immunoglobulin-fold containing bacterial adhesins: molecular and structural perspectives in host tissue colonization and infection Chatterjee, Shruti; Basak, Aditya J.; Nair, Asha V. FEMS Microbiology Letters, Vol. 368, Issue 2 https://doi.org/10.1093/femsle/fnaa220	journal	December 2020
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
Exopolysaccharide-associated protein sorting in environmental organisms: the PEP-CTERM/EpsH system. Application of a novel phylogenetic profiling heuristic Haft, Daniel H.; Paulsen, Ian T.; Ward, Naomi BMC Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1741-7007-4-29	journal	August 2006
An Antifreeze Protein Folds with an Interior Network of More Than 400 Semi-Clathrate Waters Sun, T.; Lin, F. -H.; Campbell, R. L. Science, Vol. 343, Issue 6172 https://doi.org/10.1126/science.1247407	journal	February 2014
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
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
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server Kall, L.; Krogh, A.; Sonnhammer, E. L. L. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm256	journal	May 2007
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
An ice-binding protein from an Antarctic sea ice bacterium Raymond, James A.; Fritsen, Christian; Shen, Kate FEMS Microbiology Ecology, Vol. 61, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00345.x	journal	August 2007
Dependence on epiphytic bacteria for freezing protection in an Antarctic moss,Bryum argenteum Raymond, James A. Environmental Microbiology Reports, Vol. 8, Issue 1 https://doi.org/10.1111/1758-2229.12337	journal	November 2015
Membrane translocation of proteins without hydrophobic signal peptides Kuchler, K.; Thorner, J. Current Opinion in Cell Biology, Vol. 2, Issue 4 https://doi.org/10.1016/0955-0674(90)90102-K	journal	August 1990
The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing Keeling, Patrick J.; Burki, Fabien; Wilcox, Heather M. PLoS Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pbio.1001889	journal	June 2014
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
The InterPro protein families and domains database: 20 years on Blum, Matthias; Chang, Hsin-Yu; Chuguransky, Sara Nucleic Acids Research, Vol. 49, Issue D1 https://doi.org/10.1093/nar/gkaa977	journal	November 2020
How Plants Sense and Respond to Stressful Environments Lamers, Jasper; van der Meer, Tom; Testerink, Christa Plant Physiology, Vol. 182, Issue 4 https://doi.org/10.1104/pp.19.01464	journal	March 2020
Antifreeze glycoprotein levels in Antarctic notothenioid fishes inhabiting different thermal environments and the effect of warm acclimation Jin, Yumi; DeVries, Arthur L. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 144, Issue 3 https://doi.org/10.1016/j.cbpb.2006.03.006	journal	July 2006
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Antifreeze Proteins: Structures and Mechanisms of Function Yeh, Yin; Feeney, Robert E. Chemical Reviews, Vol. 96, Issue 2 https://doi.org/10.1021/cr950260c	journal	January 1996
Genomes of the dinoflagellate Polarella glacialis encode tandemly repeated single-exon genes with adaptive functions Stephens, Timothy G.; González-Pech, Raúl A.; Cheng, Yuanyuan BMC Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12915-020-00782-8	journal	May 2020
Integrin-mediated cell adhesion: the extracellular face. Loftus, J. C.; Smith, J. W.; Ginsberg, M. H. Journal of Biological Chemistry, Vol. 269, Issue 41 https://doi.org/10.1016/S0021-9258(18)47235-3	journal	October 1994
A Semi-Quantitative, Synteny-Based Method to Improve Functional Predictions for Hypothetical and Poorly Annotated Bacterial and Archaeal Genes Yelton, Alexis P.; Thomas, Brian C.; Simmons, Sheri L. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002230	journal	October 2011
290 metagenome-assembled genomes from the Mediterranean Sea: a resource for marine microbiology Tully, Benjamin J.; Sachdeva, Rohan; Graham, Elaina D. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3558	journal	January 2017
Metagenome-assembled genomes of phytoplankton microbiomes from the Arctic and Atlantic Oceans Duncan, Anthony; Barry, Kerrie; Daum, Chris Microbiome, Vol. 10, Issue 1 https://doi.org/10.1186/s40168-022-01254-7	journal	April 2022
GeneMark.hmm: new solutions for gene finding Lukashin, A. Nucleic Acids Research, Vol. 26, Issue 4 https://doi.org/10.1093/nar/26.4.1107	journal	February 1998
Structural basis of antifreeze activity of a bacterial multi-domain antifreeze protein Wang, Chen; Pakhomova, Svetlana; Newcomer, Marcia E. PLOS ONE, Vol. 12, Issue 11 https://doi.org/10.1371/journal.pone.0187169	journal	November 2017
Evolution of prokaryotic gene order: genome rearrangements in closely related species Suyama, Mikita; Bork, Peer Trends in Genetics, Vol. 17, Issue 1 https://doi.org/10.1016/S0168-9525(00)02159-4	journal	January 2001
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Collagen-like proteins of pathogenic streptococci Lukomski, Slawomir; Bachert, Beth A.; Squeglia, Flavia Molecular Microbiology, Vol. 103, Issue 6 https://doi.org/10.1111/mmi.13604	journal	January 2017
Ice‐binding proteins and the ‘domain of unknown function’ 3494 family Vance, Tyler D. R.; Bayer‐Giraldi, Maddalena; Davies, Peter L. The FEBS Journal, Vol. 286, Issue 5 https://doi.org/10.1111/febs.14764	journal	November 2018
Predicting Protein Function by Genomic Context: Quantitative Evaluation and Qualitative Inferences Huynen, M. Genome Research, Vol. 10, Issue 8 https://doi.org/10.1101/gr.10.8.1204	journal	August 2000
Both widespread PEP-CTERM proteins and exopolysaccharides are required for floc formation of Zoogloea resiniphila and other activated sludge bacteria: PEP-CTERM protein biomarker for floc formation Gao, Na; Xia, Ming; Dai, Jingcheng Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14080	journal	March 2018
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets Steinegger, Martin; Söding, Johannes Nature Biotechnology, Vol. 35, Issue 11 https://doi.org/10.1038/nbt.3988	journal	October 2017
Ice recrystallization inhibition activity varies with ice-binding protein type and does not correlate with thermal hysteresis Gruneberg, Audrey K.; Graham, Laurie A.; Eves, Robert Cryobiology, Vol. 99 https://doi.org/10.1016/j.cryobiol.2021.01.017	journal	April 2021
The biogeochemical role of a microbial biofilm in sea ice Roukaerts, Arnout; Deman, Florian; Van der Linden, Fanny Elementa: Science of the Anthropocene, Vol. 9, Issue 1 https://doi.org/10.1525/elementa.2020.00134	journal	June 2021
Ice restructuring inhibition activities in antifreeze proteins with distinct differences in thermal hysteresis Yu, Sally O.; Brown, Alan; Middleton, Adam J. Cryobiology, Vol. 61, Issue 3 https://doi.org/10.1016/j.cryobiol.2010.10.158	journal	December 2010
Concentration-dependent oligomerization of an alpha-helical antifreeze polypeptide makes it hyperactive Mahatabuddin, Sheikh; Hanada, Yuichi; Nishimiya, Yoshiyuki Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42501	journal	February 2017
The use of gene clusters to infer functional coupling Overbeek, R.; Fonstein, M.; D'Souza, M. Proceedings of the National Academy of Sciences, Vol. 96, Issue 6 https://doi.org/10.1073/pnas.96.6.2896	journal	March 1999
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
Ice-Binding Proteins Associated with an Antarctic Cyanobacterium, Nostoc sp. HG1 Raymond, James A.; Janech, Michael G.; Mangiagalli, Marco Applied and Environmental Microbiology, Vol. 87, Issue 2 https://doi.org/10.1128/AEM.02499-20	journal	January 2021
Structure of a 1.5-MDa adhesin that binds its Antarctic bacterium to diatoms and ice Guo, Shuaiqi; Stevens, Corey A.; Vance, Tyler D. R. Science Advances, Vol. 3, Issue 8 https://doi.org/10.1126/sciadv.1701440	journal	August 2017
Hyperactive antifreeze protein from an Antarctic sea ice bacterium Colwellia sp. has a compound ice-binding site without repetitive sequences Hanada, Yuichi; Nishimiya, Yoshiyuki; Miura, Ai FEBS Journal, Vol. 281, Issue 16 https://doi.org/10.1111/febs.12878	journal	July 2014
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
Preferred crystal orientations in the fast ice along the margins of the Arctic Ocean Weeks, W. F.; Gow, A. J. Journal of Geophysical Research, Vol. 83, Issue C10 https://doi.org/10.1029/JC083iC10p05105	journal	January 1978
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
Comparative activity and functional ecology of permafrost soils and lithic niches in a hyper-arid polar desert: Ecology of Dry Valley permafrost and cryptoendoliths Goordial, Jacqueline; Davila, Alfonso; Greer, Charles W. Environmental Microbiology, Vol. 19, Issue 2 https://doi.org/10.1111/1462-2920.13353	journal	June 2016
Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions Mistry, Jaina; Finn, Robert D.; Eddy, Sean R. Nucleic Acids Research, Vol. 41, Issue 12 https://doi.org/10.1093/nar/gkt263	journal	April 2013
The chromosomal organization of horizontal gene transfer in bacteria Oliveira, Pedro H.; Touchon, Marie; Cury, Jean Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00808-w	journal	October 2017
Bacterial Diversity Assessment in Antarctic Terrestrial and Aquatic Microbial Mats: A Comparison between Bidirectional Pyrosequencing and Cultivation Tytgat, Bjorn; Verleyen, Elie; Obbels, Dagmar PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0097564	journal	June 2014
Antifreeze protein activity in Arctic cryoconite bacteria Singh, Purnima; Hanada, Yuichi; Singh, Shiv Mohan FEMS Microbiology Letters, Vol. 351, Issue 1 https://doi.org/10.1111/1574-6968.12345	journal	December 2013
Linking metagenomics to aquatic microbial ecology and biogeochemical cycles Grossart, Hans‐Peter; Massana, Ramon; McMahon, Katherine D. Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11382	journal	January 2020
Domain shuffling and the evolution of vertebrates Kawashima, Takeshi; Kawashima, Shuichi; Tanaka, Chisaki Genome Research, Vol. 19, Issue 8 https://doi.org/10.1101/gr.087072.108	journal	May 2009
In situ expression of eukaryotic ice-binding proteins in microbial communities of Arctic and Antarctic sea ice Uhlig, Christiane; Kilpert, Fabian; Frickenhaus, Stephan The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.43	journal	April 2015

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59 BASIC BIOLOGICAL SCIENCES
metagenomics
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Title: Genetic and Structural Diversity of Prokaryotic Ice-Binding Proteins from the Central Arctic Ocean.

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