Phylogenomic analysis reveals a two-stage process of the evolutionary transition of Shewanella from the upper ocean to the hadal zone.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
01
04
2020
revised:
21
06
2020
accepted:
10
07
2020
pubmed:
14
7
2020
medline:
13
5
2021
entrez:
14
7
2020
Statut:
ppublish
Résumé
Shewanella strains are characterized by versatile metabolic capabilities, resulting in their wide distribution in the ocean at different depths. Considering that particle sedimentation is an important dynamic process in the ocean, we hypothesized that hadal Shewanella species evolved from the upper ocean. In this study, we isolated three novel Shewanella strains from deep-sea sediments in the Southwest Indian Ocean. Genome sequencing indicated that strains YLB-06 and YLB-08 represent two novel species in the genus Shewanella. Through phylogenomic analysis, we showed that speciation and genomic changes in marine Shewanella strains are related to water depth. We further confirmed the aforementioned hypothesis and revealed a two-stage process of the evolutionary transition of Shewanella from the upper ocean to the hadal zone by comparative genomics and gene gain/loss analysis. Finally, the transcriptomic analysis demonstrated that recently obtained genes are strictly repressed and may thus play a minor role in the response to environmental changes.
Identifiants
pubmed: 32657519
doi: 10.1111/1462-2920.15162
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
744-756Subventions
Organisme : National Key R&D Program of China
ID : 2018YFC0309800
Organisme : National Basic Research Program of China
ID : 2015CB755901
Organisme : National Natural Science Foundation of China
ID : 91851113
Organisme : National Natural Science Foundation of China
ID : 41676118
Informations de copyright
© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Abby, S., and Daubin, V. (2007) Comparative genomics and the evolution of prokaryotes. Trends Microbiol 15: 135-141.
Aono, E., Baba, T., Ara, T., Nishi, T., Nakamichi, T., Inamoto, E., Toyonaga H., Hasegawa M., Takai Y., Okumura Y., Baba M., Tomita M., Kato C., Oshima T., Nakasone K., Mori H. (2010) Complete genome sequence and comparative analysis of Shewanella violacea, a psychrophilic and piezophilic bacterium from deep sea floor sediments. Mol Biosyst 6: 1216-1226.
Auch, A.F., Klenk, H.-P., and Göker, M. (2010) Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2: 142-148.
Besemer, J., Lomsadze, A., and Borodovsky, M. (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29: 2607-2618.
Blankenship-Williams, L.E., and Levin, L.A. (2009) Living deep: a synopsis of Hadal trench ecology. Mar Technol Soc J 43: 137-143.
Boeuf, D., Edwards, B.R., Eppley, J.M., Hu, S.K., Poff, K.E., Romano, A.E., Caron D.A., Karl D.M., DeLong E. (2019) Biological composition and microbial dynamics of sinking particulate organic matter at abyssal ocean. Proc Natl Acad Sci U S A 116: 11824-11832.
Canchaya, C., Fournous, G., Chibani-Chennoufi, S., Dillmann, M.-L., and Brüssow, H. (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6: 417-424.
Chen, S., Zhou, Y., Chen, Y., and Gu, J. (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34: i884-i890.
Consortium, T.G.O. (2019) The gene ontology resource 20 years and stillGOing strong. Nucleic Acids Res 47: D330-D338.
Csürös, M. (2010) Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 26: 1910-1912.
Eloe, E.A., Malfatti, F., Gutierrez, J., Hardy, K., Schmidt, W.E., Pogliano, K., Pogliano J., Azam F., Bartlett D.H. (2011) Isolation and characterization of a psychropiezophilic alphaproteobacterium. Appl Environ Microbiol 77: 8145-8153.
Fang, Y., Wang, Y., Liu, Z., Dai, H., Cai, H., Li, Z., et al. (2019) Multilocus sequence analysis, a rapid and accurate tool for taxonomic classification, evolutionary relationship determination, and population biology studies of the genus Shewanella. Appl Environ Microbiol 85: e02153-02118.
Fredrickson, J.K., Romine, M.F., Beliaev, A.S., Auchtung, J.M., Driscoll, M.E., Gardner, T.S., Nealson K.H., Osterman A.L., Pinchuk G., Reed J.L., Rodionov D.A., Rodrigues J.L.M., Saffarini D.A., Serres M.H., Spormann A.M., Zhulin I.B., Tiedje J.M. (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6: 592-603.
Galperin, M.Y., Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43: D261-D269.
Gao, H., Obraztova, A., Stewart, N., Popa, R., Fredrickson, J.K., Tiedje, J.M., Nealson K.H., Zhou J. (2006) Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int J Syst Evol Microbiol 56: 1911-1916.
Getz, E.W., Tithi, S.S., Zhang, L., and Aylward, F.O. (2018) Parallel evolution of genome streamlining and cellular bioenergetics across the marine radiation of a bacterial phylum. MBio 9: e01089-01018.
Giovannoni, S.J., Thrash, J.C., and Temperton, B. (2014) Implications of streamlining theory for microbial ecology. ISME J 8: 1553-1565.
Giovannoni, S.J., Tripp, H.J., Givan, S., Podar, M., Vergin, K.L., Baptista, D., Bibbs L., Eads J., Richardson T.H., Noordewier M., Rappé M.S., Short J.M., Carrington J.C., Mathur E.J. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309: 1242-1245.
Götz, S., García-Gómez, J.M., Terol, J., Williams, T.D., Nagaraj, S.H., Nueda, M.J. et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435.
Hau, H.H., and Gralnick, J.A. (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61: 237-258.
Ibarbalz, F.M., Henry, N., Brandão, M.C., Martini, S., Busseni, G., Byrne, H., Coelho L.P., Endo H., Gasol J.M., Gregory A.C., Mahé F., Rigonato J., Royo-Llonch M., Salazar G., Sanz-Sáez I., Scalco E., Soviadan D., Zayed A.A., Zingone A., Labadie K., Ferland J., Marec C., Kandels S., Picheral M., Dimier C., Poulain J., Pisarev S., Carmichael M., Pesant S., Babin M., Boss E., Iudicone D., Jaillon O., Acinas S.G., Ogata H., Pelletier E., Stemmann L., Sullivan M.B., Sunagawa S., Bopp L., de Vargas C., Karp-Boss L., Wincker P., Lombard F., Bowler C., Zinger L., Acinas S.G., Babin M., Bork P., Boss E., Bowler C., Cochrane G., de Vargas C., Follows M., Gorsky G., Grimsley N., Guidi L., Hingamp P., Iudicone D., Jaillon O., Kandels S., Karp-Boss L., Karsenti E., Not F., Ogata H., Pesant S., Poulton N., Raes J., Sardet C., Speich S., Stemmann L., Sullivan M.B., Sunagawa S., Wincker P. (2019) Global trends in marine plankton diversity across kingdoms of life. Cell 179: 1084-1097.
Ichino, M.C., Clark, M.R., Drazen, J.C., Jamieson, A., Jones, D.O.B., Martin, A.P., et al. (2015) The distribution of benthic biomass in hadal trenches: a modelling approach to investigate the effect of vertical and lateral organic matter transport to the seafloor. Deep-Sea Res I Oceanogr Res Pap 100: 21-33.
Jamieson, A. (2015) The Hadal Zone: Life in the Deepest Oceans. UK: Cambridge University Press.
Jamieson, A.J. (2001) Ecology of deep oceans: Hadal trenches. In eLS, Chichester, UK: John Wiley & Sons.
Jamieson, A.J., Fujii, T., Mayor, D.J., Solan, M., and Priede, I.G. (2010) Hadal trenches: the ecology of the deepest places on Earth. Trends Ecol Evol 25: 190-197.
Jian, H., Xu, G., Gai, Y., Xu, J., and Xiao, X. (2016) The histone-like nucleoid structuring protein (H-NS) is a negative regulator of the lateral flagellar system in the deep-sea bacterium Shewanella piezotolerans WP3. Appl Environ Microbiol 82: 2388-2398.
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., and Hattori, M. (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277-D280.
Kim, D., Langmead, B., and Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12: 357-360.
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547-1549.
Kusube, M., Kyaw, T.S., Tanikawa, K., Chastain, R.A., Hardy, K.M., Cameron, J., and Bartlett, D.H. (2017) Colwellia marinimaniae sp. nov., a hyperpiezophilic species isolated from an amphipod within the challenger deep, Mariana trench. Int J Syst Evol Microbiol 67: 824-831.
Lagesen, K., Hallin, P., Rødland, E.A., Staerfeldt, H.-H., Rognes, T., and Ussery, D.W. (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100-3108.
Lan, Y., Morrison, J.C., Hershberg, R., and Rosen, G.L. (2014) POGO-DB-a database of pairwise-comparisons of genomes and conserved orthologous genes. Nucleic Acids Res 42: D625-D632.
Lauro, F.M., Chastain, A., Ferriera, S., Johnson, J., Yayanos, A.A., and Bartlett, D.H. (2013) Draft genome sequence of the Deep-Sea bacterium Shewanella benthica strain KT99. Genome Announc 1: e00210-00213.
Lawrence, J.G., and Hendrickson, H. (2005) Genome evolution in bacteria: order beneath chaos. Curr Opin Microbiol 8: 572-578.
Li, B., and Dewey, C.N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
Li, L. Jr., C.J.S., and Roos, D.S. (2003) OrthoMCL: identification of Ortholog groups for eukaryotic genomes Genome Res 13: 2178-2189.
Liu, J., Zheng, Y., Lin, H., Wang, X., Li, M., Liu, Y., Yu M., Zhao M., Pedentchouk N., Lea-Smith D.J., Todd J.D., Magill C.R., Zhang W.J., Zhou S., Song D., Zhong H., Xin Y., Yu M., Tian J., Zhang X.H. (2019) Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench. Microbiome 7: 47.
Lowe, T.M., and Eddy, S.R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
Maruyama, A., Honda, D., Yamamoto, H., Kitamura, K., and Higashihara, T. (2000) Phylogenetic analysis of psychrophilic bacteria isolated from the Japan Trench, including a description of the deep-sea species Psychrobacter pacificensis sp. nov. Int J Syst Evol Microbiol 50: 835-846.
Nogi, Y., Hosoya, S., Kato, C., and Horikoshi, K. (2004) Colwellia piezophila sp. nov., a novel piezophilic species from deep-sea sediments of the Japan Trench. Int J Syst Evol Microbiol 54: 1627-1631.
Nogi, Y., and Kato, C. (1999) Taxonomic studies of extremely barophilic bacteria isolated from the Mariana Trench and description of Moritella yayanosii sp. nov., a new barophilic bacterial isolate. Extremophiles 3: 71-77.
Nogi, Y., Kato, C., and Horikoshi, K. (1998) Taxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanella violacea sp. nov. Arch Microbiol 170: 331-338.
Nunoura, T., Takaki, Y., Hirai, M., Shimamura, S., Makabe, A., Koide, O., Kikuchi T., Miyazaki J., Koba K., Yoshida N., Sunamura M., Takai K. (2015) Hadal biosphere: insight into the microbial ecosystem in the deepest ocean on earth. Proc Natl Acad Sci U S A 112: E1230-E1236.
Orcutt, B.N., Sylvan, J.B., Knab, N.J., and Edwards, K.J. (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75: 361-422.
Price, M.N., Dehal, P.S., and Arkin, A.P. (2010) FastTree 2 - approximately maximum-likelihood Treesfor large alignments. PLoS One 5: e9490.
Qin, Q.-L., Li, Y., Sun, L.-L., Wang, Z.-B., Wang, S., Chen, X.-L., et al. (2019) Trophic specialization results in genomic reduction in free-living marine Idiomarina bacteria. MBio 10: e02545-02518.
Richter, M., and Rosselló-Móra, R. (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126-19131.
Robinson, M.D., McCarthy, D.J., and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
Salcher, M.M., Schaefle, D., Kaspar, M., Neuenschwander, S.M., and Ghai, R. (2019) Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae. ISME J 13: 2764-2777.
Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez R., McWilliam H., Remmert M., Söding J., Thompson J.D., Higgins D.G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
Singh, P., Raghukumar, C., Verma, A.K., and Meena, R.M. (2012) Differentially expressed genes under simulated deep-sea conditions in the psychrotolerant yeast Cryptococcus sp. NIOCC#PY13. Extremophiles 16: 777-785.
Soutourina, O.A., and Bertin, P.N. (2003) Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol Rev 27: 505-523.
Stackebrandt, E., Frederiksen, W., Garrity, G.M., Grimont, P.A.D., Kümpfer, P., Maiden, M.C.J., et al. (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52: 1043-1047.
Sunagawa, S., Coelho, L.P., Chaffron, S., Kultima, J.R., Labadie, K., Salazar, G., Djahanschiri B., Zeller G., Mende D.R., Alberti A., Cornejo-Castillo F.M., Costea P.I., Cruaud C., d'Ovidio F., Engelen S., Ferrera I., Gasol J.M., Guidi L., Hildebrand F., Kokoszka F., Lepoivre C., Lima-Mendez G., Poulain J., Poulos B.T., Royo-Llonch M., Sarmento H., Vieira-Silva S., Dimier C., Picheral M., Searson S., Kandels-Lewis S., Tara Oceans coordinators, Bowler C., de Vargas C., Gorsky G., Grimsley N., Hingamp P., Iudicone D., Jaillon O., Not F., Ogata H., Pesant S., Speich S., Stemmann L., Sullivan M.B., Weissenbach J., Wincker P., Karsenti E., Raes J., Acinas S.G., Bork P., Boss E., Bowler C., Follows M., Karp-Boss L., Krzic U., Reynaud E.G., Sardet C., Sieracki M., Velayoudon D. (2015) Structure and function of the global ocean microbiome. Science 348: 1261359.
Thorell, K., Meier-Kolthoff, J.P., Sjöling, Å., and Martín-Rodríguez, A.J. (2019) Whole-genome sequencing redefines Shewanella taxonomy. Front Microbiol 10: 01861.
Toffin, L., Bidault, A., Pignet, P., Tindall, B.J., Slobodkin, A., Kato, C., and Prieur, D. (2004) Shewanella profunda sp. nov., isolated from deep marine sediment of the Nankai Trough. Int J Syst Evol Microbiol 54: 1943-1949.
Touchon, M., Sousa, J.A.M.d., and Rocha, E.P. (2017) Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Curr Opin Microbiol 38: 66-73.
Wang, F., Wang, P., Chen, M., and Xiao, X. (2004) Isolation of extremophiles with the detection and retrieval of Shewanella strains in deep-sea sediments from the west Pacific. Extremophiles 8: 165-168.
Wang, H., and Sun, L. (2017) Comparative metagenomics reveals insights into the deep-sea adaptation mechanism of the microorganisms in Iheya hydrothermal fields. World J Microbiol Biotechnol 33: 86.
Wang, L., Feng, Z., Wang, X., Wang, X., and Zhang, X. (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
Wang, Y., Huang, J.-M., Cui, G.-J., Nunoura, T., Takaki, Y., Li, W.-L., Li J., Gao Z.M., Takai K., Zhang A.Q., Stepanauskas R. (2019) Genomics insights into ecotype formation of ammonia-oxidizing archaea in the deep ocean. Environ Microbiol 21: 716-729.
Wei, Y., Fang, J., Xu, Y., Zhao, W., and Cao, J. (2018) Corynebacterium hadale sp. nov. isolated from hadopelagic water of the New Britain Trench. Int J Syst Evol Microbiol 68: 1474-1478.
Xiao, X., Wang, P., Zeng, X., Bartlett, D.H., and Wang, F. (2007) Shewanella psychrophila sp. nov. and Shewanella piezotolerans sp. nov., isolated from west Pacific deep-sea sediment. Int J Syst Evol Microbiol 57: 60-65.
Yin, Q., Zhang, W., Li, X., Zhou, L., Qi, X., Zhang, C., and Wu, L.-F. (2019) Contribution of trimethylamine N-oxide on the growth and pressure tolerance of deep-sea bacteria. J Oceanol Limnol 37: 210-222.
Yu, L., Tang, X., Wei, S., Qiu, Y., Xu, X., Xu, G., Wang Q., Yang Q. (2019b) Two novel species of the family Bacillaceae: Oceanobacillus piezotolerans sp. nov. and Bacillus piezotolerans sp. nov., from deep-sea sediment samples of Yap Trench. Int J Syst Evol Microbiol 69: 3022-3030.
Yu, L., Zhou, Z., Wei, S., Xu, X., Wang, Q., Xu, G., Tang X., Yang Q. (2019a) Marinomonas piezotolerans sp. nov., isolated from deep-sea sediment of the Yap Trench, Pacific Ocean. Int J Syst Evol Microbiol 69: 739-744.
Zhang, S.-D., Santini, C.-L., Zhang, W., Barbe, V., Mangenot, S., Guyomar, C. et al. (2016) Genomic and physiological analysis reveals versatile metabolic capacity of deep-sea Photobacterium phosphoreum ANT-2200. Extremophiles 20: 301-310.
Zhang, W., Cui, X., Chen, L., Yang, J., Li, X., Zhang, C., et al. (2019) Complete genome sequence of Shewanella benthica DB21MT-2, an obligate piezophilic bacterium isolated from the deepest Mariana Trench sediment. Mar Genomics 44: 52-56.