Two Strains of Crocosphaera watsonii with Highly Conserved Genomes are Distinguished by Strain-Specific Features
Open accessAbstract
Unicellular nitrogen-fixing cyanobacteria are important components of marine phytoplankton. Although non-nitrogen-fixing marine phytoplankton generally exhibit high gene sequence and genomic diversity, gene sequences of natural populations and isolated strains of Crocosphaerawatsonii, one of the two most abundant open ocean unicellular cyanobacteria groups, have been shown to be 98-100% identical. The low sequence diversity in Crocosphaera is a dramatic contrast to sympatric species of Prochlorococcus and Synechococcus, and raises the question of how genome differences can explain observed phenotypic diversity among Crocosphaera strains. Here we show, through whole genome comparisons of two phenotypically different strains, that there are strain-specific sequences in each genome, and numerous genome rearrangements, despite exceptionally low sequence diversity in shared genomic regions. Some of the strain-specific sequences encode functions that explain observed phenotypic differences, such as exopolysaccharide biosynthesis. The pattern of strain-specific sequences distributed throughout the genomes, along with rearrangements in shared sequences is evidence of significant genetic mobility that may be attributed to the hundreds of transposase genes found in both strains. Furthermore, such genetic mobility appears to be the main mechanism of strain divergence in Crocosphaera which do not accumulate DNA microheterogeneity over the vast majority of their genomes. The strain-specific sequences found in this study provide tools for future physiological studies, as well as genetic markers to help determine the relative abundance of phenotypes in natural populations.
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Previous studies have shown that a large proportion of transposases and RTase constituted long repeated sequences in some cyanobacteria.
“Previous studies have shown that a large proportion of the transposases and RTase constituted the long repeated sequences in some cyanobacteria.57–60”
From Whole genomic DNA sequencing and comparative genomic analysis of<i>Arthrospira platensis</i>: high genome plasticity and genetic diversity (2016) · cites this paper as [57]
Materials and Methods (Transposase annotation; page unavailable) describes highly repetitive ORFs in the cyanobacterium Crocosphaera watsonii that were reassessed as transposase genes. Results and Discussion (Transposase gene comparisons; page unavailable) reports many identical copies of transposase sequences. The paper does not establish that these are long repeated sequences or address RTase, so those parts of the claim are unsupported. (LLM, conf=0.85)
Experimental — accuracy not yet measuredDuplicated genes were usually adjacently located or duplication-linked with many unknown functions, some annotated by one or two of RTase, transposase, and integrase, and duplicated fragments varied in size from several to dozens of kilobases.
“Another significant characteristic of duplicated genes was that they were usually adjacently located or duplication-linked with a plenty of unknown functions, some of which can be annotated by one or two of the three enzymes (RTase, transposase, and integrase), and these duplicated fragments varied in size from several to dozens of kilobases.57–59”
From Whole genomic DNA sequencing and comparative genomic analysis of<i>Arthrospira platensis</i>: high genome plasticity and genetic diversity (2016) · cites this paper as [57]
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“…high abundances using qPCR and direct cell counts (Zehr et al., 2001; Falcon et al., 2004; Church et al., 2005a, 2008; Langlois et al., 2008; Moisander et al., 2008, 2010), and measured high rates of in situ unicellular cyanobacterial N2 fixation (Zehr et al., 2001; Falcon et al., 2004;…”
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“…which are dominated by cyanobacteria in most of the world’s open oceans, are important in global marine biogeochemical cycles and account for half of global carbon fixation (Waterbury et al., 1986; Goericke and Welschmeyer, 1993; Liu et al., 1997; Partensky et al., 1999; Scanlan and West, 2002).”
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“Surveys of the C. watsonii nitrogenase gene nifH also showed very little, if any, sequence variation in either the Atlantic (Langlois et al., 2005) or the Pacific Oceans (Church et al., 2005a,b).”
BackgroundInfluentialRegional distributions of nitrogen‐fixing bacteria in the Pacific Ocean
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“However, more recent studies have reported high abundances using qPCR and direct cell counts (Zehr et al., 2001; Falcon et al., 2004; Church et al., 2005a, 2008; Langlois et al., 2008; Moisander et al., 2008, 2010), and measured high rates of in situ unicellular cyanobacterial N2 fixation (Zehr et…”
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“…regions, phytoplankton production is often limited by nutrients, especially nitrogen (N), and in those areas, nitrogen (N2) fixation provides an important source of new N that supports primary productivity (Karl et al., 1997, 2002; Bonnet et al., 2009; Kitajima et al., 2009; Shiozaki et al., 2010).”
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“…Langlois et al., 2008; Moisander et al., 2008, 2010), and measured high rates of in situ unicellular cyanobacterial N2 fixation (Zehr et al., 2001; Falcon et al., 2004; Montoya et al., 2004; Kitajima et al., 2009; Moisander et al., 2010), demonstrating that unicellular diazotrophs are often…”
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“…sequence conservation in Crocosphaera strains also contrasts with sequence divergence observed in the sympatric, non-N2-fixing cyanobacteria Prochlorococcus and Synechococcus (Rocap et al., 2002; Ernst et al., 2003; Brown and Fuhrman, 2005; Rusch et al., 2007; Partensky and Garczarek, 2010).”
BackgroundInfluentialPhosphorus Scavenging in the Unicellular Marine Diazotroph Crocosphaera watsonii
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“phenotypic differences with ecological implications, such as the possible absence of phosphorus scavenging genes in some strains (Dyhrman and Haley, 2006), and differences in cell size, temperature growth optima, exopolysaccharide (EPS) production, and N2 fixation rates (Webb et al.”
BackgroundInsertion Sequence Diversity in Archaea
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“Transposons are highly abundant mobile genetic elements that mediate genome shuffling within and among all domains of life (Mahillon et al., 1999; Lander et al., 2001; Feschotte et al., 2002; Waterston et al., 2002; Goodchild et al., 2004; Filee et al., 2007; Touchon and Rocha, 2007; Aziz et al., 2010).”
BackgroundDinitrogen fixation in the world’s oceans
Karl, D. M., Michaels, A. F., Bergman, B., Capone, D., Carpenter, E., Letelier, R. M., Lipschultz, F., Paerl, H. W., Sigman, D. M., & Stal, L. J. (2002) · Springer eBooks · doi:10.1007/978-94-017-3405-9_2 · Cited by 140 · see citing works
Marine bacterial microdiversity as revealed by internal transcribed spacer analysis
Brown, M., & Fuhrman, J. A. (2005) · Aquatic Microbial Ecology · doi:10.3354/ame041015 · Cited by 139 · cited 9× · see citing works
“…sequence conservation in Crocosphaera strains also contrasts with sequence divergence observed in the sympatric, non-N2-fixing cyanobacteria Prochlorococcus and Synechococcus (Rocap et al., 2002; Ernst et al., 2003; Brown and Fuhrman, 2005; Rusch et al., 2007; Partensky and Garczarek, 2010).”
BackgroundInfluentialNew estimation of N2 fixation in the western and central Pacific Ocean and its marginal seas
Shiozaki, T., Furuya, K., Kodama, T., Kitajima, S., Takeda, S., Takemura, T., & Kanda, J. (2010) · Global Biogeochemical Cycles · doi:10.1029/2009gb003620 · Cited by 127 · see citing works
Webb, E. A., Ehrenreich, I. M., Brown, S. L., Valois, F. W., & Waterbury, J. B. (2008) · Environmental Microbiology · doi:10.1111/j.1462-2920.2008.01771.x · Cited by 125 · cited 6× · see citing works
“For the taxonomic analysis of the WH0003 ORFs least similar to WH8501, sequences were placed into three bins based on tID of the best BLAST alignment (35–50% tID,20–35% tID,and 20% tID).”
BackgroundMethodInfluential[6] Isolation and growth of marine planktonic cyanobacteria
Waterbury, J. B., & Willey, J. M. (1988) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(88)67009-1 · Cited by 122 · cited 1× · see citing works
“A non-axenic culture of C. watsonii WH0003 was grown in nitrogen-free SO medium (Waterbury et al., 1986, 1988) in polycarbonate tissue culture flasks with a 0.2 μm pore-size vent cap (Corning Inc., Corning, NY, USA) at 26˚C under a 12:12 h light/dark cycle.”
MethodInfluentialKitajima, S., Furuya, K., Hashihama, F., Takeda, S., & Kanda, J. (2009) · Limnology and Oceanography · doi:10.4319/lo.2009.54.2.0537 · Cited by 119 · cited 3× · see citing works
“…regions, phytoplankton production is often limited by nutrients, especially nitrogen (N), and in those areas, nitrogen (N2) fixation provides an important source of new N that supports primary productivity (Karl et al., 1997, 2002; Bonnet et al., 2009; Kitajima et al., 2009; Shiozaki et al., 2010).”
BackgroundInfluentialIS elements as constituents of bacterial genomes
Mahillon, J., Leonard, C. A., & Chandler, M. (1999) · Research in Microbiology · doi:10.1016/s0923-2508(99)00124-2 · Cited by 117 · cited 2× · see citing works
“Transposons are highly abundant mobile genetic elements that mediate genome shuffling within and among all domains of life (Mahillon et al., 1999; Lander et al., 2001; Feschotte et al., 2002; Waterston et al., 2002; Goodchild et al., 2004; Filee et al., 2007; Touchon and Rocha, 2007; Aziz et al., 2010).”
BackgroundShi, T., Shilova, I. N., Rabouille, S., & Zehr, J. P. (2010) · The ISME Journal · doi:10.1038/ismej.2009.148 · Cited by 113 · cited 2× · see citing works
“The majority of these genes showed diel expression patterns (listed in right column of Table S3 in Supplementary Material) in a previous microarray study (Shi et al., 2010).”
BackgroundMethodSelf-citationRegulation of the initiation of chromosomal replication in bacteria
Zakrzewska‐Czerwińska, J., Jakimowicz, D., Zawilak-Pawlik, A. M., & Messer, W. (2007) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2007.00070.x · Cited by 108 · see citing works
Dyhrman, S. T., Haley, S. T., Birkeland, S. R., Wurch, L. L., Cipriano, M. J., & McArthur, A. G. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.72.1.252-260.2006 · Cited by 87 · see citing works
Single-Stranded DNA Transposition Is Coupled to Host Replication
Ton‐Hoang, B., Pasternak, C., Siguier, P., Guynet, C., Hickman, A. B., Dyda, F., Sommer, S., & Chandler, M. (2010) · Cell · doi:10.1016/j.cell.2010.06.034 · Cited by 82 · cited 1× · see citing works
“…protein (Messer, 2002; Zakrzewska-Czerwinska et al., Frontiers in Microbiology | Aquatic Microbiology December 2011 | Volume 2 | Article 261 | 10 2007) suggests that transposase expression may be coordinated with DNA replication as has been observed in other organisms (Ton-Hoang et al., 2010).”
BackgroundHewson, I., Poretsky, R. S., Beinart, R. A., White, A., Shi, T., Bench, S. R., Moisander, P. H., Paerl, R. W., Tripp, H. J., Montoya, J. P., et al. (2009) · The ISME Journal · doi:10.1038/ismej.2009.8 · Cited by 82 · see citing works
Self-citationLow genomic diversity in tropical oceanic N 2 -fixing cyanobacteria
Zehr, J. P., Bench, S. R., Mondragon, E. A., McCarren, J., & DeLong, E. F. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701017104 · Cited by 75 · cited 8× · see citing works
“The genome conservation observed in the two Crocosphaera genomes described in this study and the previously described environmental sequences (Zehr et al., 2007) could be explained using three possible mechanisms.”
BackgroundResultInfluentialSelf-citationGoodchild, A., Raftery, M. J., Saunders, N. F. W., Guilhaus, M., & Cavicchioli, R. (2004) · Journal of Proteome Research · doi:10.1021/pr0498988 · Cited by 73 · cited 2× · see citing works
“Transposons are highly abundant mobile genetic elements that mediate genome shuffling within and among all domains of life (Mahillon et al., 1999; Lander et al., 2001; Feschotte et al., 2002; Waterston et al., 2002; Goodchild et al., 2004; Filee et al., 2007; Touchon and Rocha, 2007; Aziz et al., 2010).”
BackgroundProchlorococcus, a marine photosynthetic prokaryote of global significance
Partensky, F., Hess, W., & Vaulot, D. (1999) · FreiDok plus (Universitätsbibliothek Freiburg) · Cited by 32 · see citing works
(2000) · Time to knit · doi:10.1016/s0967-0653(97)81036-8 · Cited by 25 · see citing works
Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus
Scanlan, D. J. (2002) · FEMS Microbiology Ecology · doi:10.1016/s0168-6496(01)00217-3 · Cited by 24 · see citing works
Positive Selection on Transposase Genes of Insertion Sequences in the Crocosphaera watsonii Genome
Mes, T. H. M., & Doeleman, M. (2006) · Journal of Bacteriology · doi:10.1128/jb.01021-06 · Cited by 18 · cited 2× · see citing works
“watsonii WH8501 draft genome, when the unusually high abundance of transposase genes was recognized, and evidence was found for positive evolutionary selection in a subset of those genes (Mes and Doeleman, 2006).”
BackgroundComparative molecular population genetics of phycoerythrin locus in Prochlorococcus
Zhao, F., & Qin, S. (2006) · Genetica · doi:10.1007/s10709-006-0010-9 · Cited by 13 · cited 5× · see citing works
“As direct descendents of ancient phototrophs with deeply rooted phylogenies, it is not surprising that cyanobacteria typically show a large amount of genomic sequence heterogeneity, even among closely related species (Zhao and Qin, 2007; Dufresne et al., 2008).”
BackgroundResultInfluentialMoisander, P. H., Beinart, R. A., Voß, M., et al. (2008) · The ISME Journal · doi:10.1038/ismej.2008.84 · Cited by 5 · see citing works
(2000) · Time to knit · doi:10.1016/s0967-0653(97)87682-x · Cited by 4 · see citing works
Flagged first, then by citations
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Improving the coverage of the cyanobacterial phylum using diversity driven genome sequencing
Shih, P. M., Wu, D., Latifi, A., Axen, S. D., Fewer, D. P., Talla, E., Calteau, A., Cai, F., Tandeau de Marsac, N., Rippka, R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217107110 · Cited by 800 · see citing works
Soil microbial trait-based strategies drive metabolic efficiency along an altitude gradient
Feng, J., Zeng, X., Zhang, Q., Zhou, X., Liu, Y., & Huang, Q. (2021) · ISME Communications · doi:10.1038/s43705-021-00076-2 · Cited by 178 · see citing works
“These results indicate that microbial classification based on higher phylogenetic levels (such as at the order or phylum levels) have limitations in explaining community-level physiological strategies, because taxonomically related strains can have divergent features, while dissimilar strains may exhibit identical tra…”
BackgroundWilson, S. T., Aylward, F. O., Ribalet, F., Barone, B., Casey, J. R., Connell, P. E., Eppley, J. M., Ferrón, S., Fitzsimmons, J. N., Hayes, C. T., et al. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.118 · Cited by 144 · see citing works
Self-citationLuo, E., Eppley, J. M., Romano, A. E., Mende, D. R., & DeLong, E. F. (2020) · The ISME Journal · doi:10.1038/s41396-020-0604-8 · Cited by 103 · see citing works
Mareš, J., Johansen, J. R., Hauer, T., Zima, J., Ventura, S., Cuzman, O. A., Tiribilli, B., & Kaštovský, J. (2019) · Journal of Phycology · doi:10.1111/jpy.12853 · Cited by 92 · see citing works
“Several isolates designated as Cyanothece sp. and C. watsonii were subjected to whole genome sequencing and phylogenomic studies (Zehr et al. 2007, Welsh et al. 2008, Bench et al. 2011, Shih et al. 2013).”
MethodBombar, D., Heller, P., Sánchez-Baracaldo, P., Carter, B. J., & Zehr, J. (2014) · The ISME Journal · doi:10.1038/ismej.2014.167 · Cited by 88 · see citing works
Self-citationVoß, B., Bolhuis, H., Fewer, D. P., Kopf, M., Möke, F., Haas, F. B., El‐Shehawy, R. M., Hayes, P. K., Bergman, B., Sivonen, K., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060224 · Cited by 89 · see citing works
Rhizobia–diatom symbiosis fixes missing nitrogen in the ocean
Tschitschko, B., Esti, M., Philippi, M., Kidane, A. T., Littmann, S., Kitzinger, K., Speth, D. R., Li, S., Kraberg, A. C., Tienken, D., et al. (2024) · Nature · doi:10.1038/s41586-024-07495-w · Cited by 83 · see citing works
Sohm, J. A., Edwards, B. R., Wilson, B. G., & Webb, E. A. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00229 · Cited by 81 · see citing works
In situ identification and N2 and C fixation rates of uncultivated cyanobacteria populations
Krupke, A., Musat, N., LaRoche, J., Mohr, W., Fuchs, B. M., Amann, R., Kuypers, M. M. M., & Foster, R. A. (2013) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2013.02.002 · Cited by 76 · see citing works
High abundance and expression of transposases in bacteria from the Baltic Sea
Vigil-Stenman, T., Ininbergs, K., Bergman, B., & Ekman, M. (2017) · The ISME Journal · doi:10.1038/ismej.2017.114 · Cited by 75 · see citing works
“…transposase frequencies recorded are from the free-living Cyanobacteria Microcystis aeruginosa (Kaneko et al., 2007), and Crocosphaera watsonii (Bench et al., 2011), Correspondence: M Ekman, Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm SE-106 91,…”
BackgroundInfluentialCaputo, A., Nylander, J. A. A., & Foster, R. A. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fny297 · Cited by 62 · see citing works
Foster, R. A., Sztejrenszus, S. Y., & Kuypers, M. M. M. (2013) · Journal of Phycology · doi:10.1111/jpy.12057 · Cited by 61 · see citing works
“Currently, there are up to 10 different strains of C. watsonii isolated from the open ocean (Atlantic and Pacific Oceans; Webb et al. 2009) which possess great phenotypic plasticity while maintaining high genetic conservation (Zehr et al. 2007b, Webb et al. 2009, Bench et al. 2011).”
BackgroundCellular interactions: lessons from the nitrogen‐fixing cyanobacteria
Thompson, A., & Zehr, J. P. (2013) · Journal of Phycology · doi:10.1111/jpy.12117 · Cited by 59 · see citing works
Self-citationWhole genome comparison of six C rocosphaera watsonii strains with differing phenotypes
Bench, S. R., Heller, P., Frank, I. E., Arciniega, M., Shilova, I. N., & Zehr, J. P. (2013) · Journal of Phycology · doi:10.1111/jpy.12090 · Cited by 54 · see citing works
“Although these strains exhibit phenotypic differences, genetic comparisons have found the vast majority of DNA sequences to be essentially identical among cultivated strains and environmental sequences (Zehr et al. 2007, Bench et al. 2011).”
BackgroundMethodInfluentialSelf-citationReconstructing the complex evolutionary history of mobile plasmids in red algal genomes
Lee, J., Kim, K. M., Yang, E. C., Miller, K. A., Boo, S. M., Bhattacharya, D., & Yoon, H. S. (2016) · Scientific Reports · doi:10.1038/srep23744 · Cited by 48 · see citing works
Walworth, N. G., Pfreundt, U., Nelson, W. C., Mincer, T. J., Heidelberg, J. F., Fu, F., Waterbury, J. B., del Rio, T. G., Goodwin, L., Kyrpides, N. C., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1422332112 · Cited by 45 · see citing works
“These include photosynthetic free-living forms, such as the filamentous Trichodesmium and the unicellular Crocosphaera and Cyanothece, and photosynthetic and nonphotosynthetic symbiotic forms, such as heterocystous Richelia and Candidatus Atelocyanobacterium thalassa (3, 5, 17).”
BackgroundInfluentialXu, T., Qin, S., Hu, Y., Song, Z., Ying, J., Li, P., Dong, W., Zhao, F., Yang, H., & Bao, Q. (2016) · DNA Research · doi:10.1093/dnares/dsw023 · Cited by 37 · see citing works
Zhang, M., Bai, X., Wang, Y., Li, Y., Cui, Y., Hu, S., Jonathan, M. A., Dong, L., & Yu, X. (2022) · CATENA · doi:10.1016/j.catena.2022.106894 · Cited by 38 · see citing works
Bertin, C., Pau‐Roblot, C., Courtois, J., Manso-Silván, L., Tardy, F., Poumarat, F., Citti, C., Sirand‐Pugnet, P., Gaurivaud, P., & Thiaucourt, F. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.02892-14 · Cited by 38 · see citing works
“This is no exception to other prokaryotes, as genes for polysaccharide synthesis are often carried by mobile genetic elements, such as plasmids in lactococci (39), or are closely associated to insertion sequences, as in Desulfovibrio (40), Lactococcus (41), or Crocosphaera (42).”
BackgroundEcological and evolutionary genomics of marine photosynthetic organisms
Coelho, S. M., Simon, N., Ahmed, S., Cock, J. M., & Partensky, F. (2012) · Molecular Ecology · doi:10.1111/mec.12000 · Cited by 31 · see citing works
“These are particularly abundant in the two genomes of C. watsonii sequenced so far (strains WH8501 and WH0003), with e.g. a total of 1,211 in the former strain, including 292 copies of a single transposase sequence (Bench et al. 2011; Larsson et al. 2011).”
BackgroundInfluentialThe future of genomics in polar and alpine cyanobacteria
Chrismas, N. A. M., Anesio, A. M., & Sánchez‐Baracaldo, P. (2018) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiy032 · Cited by 24 · see citing works
Bombar, D., Taylor, C. D., Wilson, S. T., Robidart, J. C., Rabines, A. J., Turk‐Kubo, K. A., Kemp, J. N., Karl, D. M., & Zehr, J. P. (2015) · Journal of Plankton Research · doi:10.1093/plankt/fbv049 · Cited by 23 · see citing works
Self-citationBench, S. R., Frank, I. E., Robidart, J. C., & Zehr, J. P. (2015) · Environmental Microbiology · doi:10.1111/1462-2920.13180 · Cited by 18 · see citing works
Self-citationl-Lactate treatment by photosynthetic cyanobacteria expressing heterogeneous l-lactate dehydrogenase
Kato, Y., Inabe, K., Haraguchi, Y., Shimizu, T., Kondo, A., & Hasunuma, T. (2023) · Scientific Reports · doi:10.1038/s41598-023-34289-3 · Cited by 16 · see citing works
Qu, P., Fu, F., Wang, X., Kling, J. D., Elghazzawy, M., Huh, M., Zhou, Q., Wang, C., Mak, E. W. K., Lee, M. D., et al. (2022) · Environmental Microbiology Reports · doi:10.1111/1758-2229.13041 · Cited by 17 · see citing works
Enhanced carbon use efficiency and warming resistance of soil microorganisms under organic amendment
Li, L., Li, C., Guo, H., Liu, Y., Sheng, J., Guo, S., Shen, Q., Ling, N., & Guo, J. (2024) · Environment International · doi:10.1016/j.envint.2024.109043 · Cited by 16 · see citing works
Crocosphaera watsonii – A widespread nitrogen‐fixing unicellular marine cyanobacterium
Masuda, T., Mareš, J., Shiozaki, T., Inomura, K., Fujiwara, A., & Prášil, O. (2024) · Journal of Phycology · doi:10.1111/jpy.13450 · Cited by 15 · see citing works
“…high number of transposases (Bench et al., 2011, 2013; Hewson et al., 2009; Mes & Doeleman, 2006; Zehr et al., 2007), suggesting a mechanism for adaptation to changing environmental conditions, which could underpin the variety of phenotypic differences observed among strains (Bench et al., 2011).”
Marine Nitrogen Fixation: Organisms, Significance, Enigmas, and Future Directions
Zehr, J. P., & Bombar, D. (2015) · Biological nitrogen fixation · doi:10.1002/9781119053095.ch84 · Cited by 14 · see citing works
Self-citationDreher, T. W., Matthews, R., Davis, E. W., & Mueller, R. (2023) · Harmful Algae · doi:10.1016/j.hal.2023.102433 · Cited by 11 · see citing works
Genomics of algae: Its challenges and applications
Minhas, A. P., Kaur, B., & Kaur, J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817076-2.00013-5 · Cited by 9 · see citing works
Harnessing Solar‐Powered Oxic N 2 ‐fixing Cyanobacteria for the BioNitrogen Economy
Young, J. S., Gu, L., Gibbons, W. R., & Zhou, R. (2021) · doi:10.1002/9783527824908.ch13 · Cited by 9 · see citing works
Wilbanks, E. G., Salman-Carvalho, V., Jaekel, U., Humphrey, P. T., Eisen, J. A., Buckley, D. H., & Zinder, S. H. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01623 · Cited by 7 · see citing works
“These findings confirm that GB-CYN1 resembles free-living Chroococcales of the clades B and C (Welsh et al., 2008; Bandyopadhyay et al., 2011; Bench et al., 2011, 2013) rather than the metabolically streamlined, endosymbiotic UCYN-A clade (Zehr et al., 2008; Tripp et al., 2010; Thompson et al.,…”
BackgroundIsolation and biogeography of the oligotrophic ocean diazotroph, Crocosphaera waterburyi nov. sp
Cleveland, C. S., Turk-Kubo, K. A., Zhao, Y., Zehr, J. P., & Webb, E. A. (2024) · The ISME Journal · doi:10.1093/ismejo/wrae217 · Cited by 5 · see citing works
“Different C.watsonii isolates have been shown to display strain-specific differences in cell size and exopolysaccharide (EPS) production [5, 63].”
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Zehr, J. P., & Capone, D. G. (2021) · Springer eBooks · doi:10.1007/978-3-030-67746-6_4 · Cited by 3 · see citing works
Self-citationZehr, J. P., Foster, R. A., Waterbury, J., & Webb, E. A. (2022) · Bergey's Manual of Systematics of Archaea and Bacteria · doi:10.1002/9781118960608.gbm01517 · Cited by 2 · see citing works
Self-citationZhang, W., Li, W., Zhuolin, L. I., Li, X. Y., Duan, R., Luo, D., Xiong, G., Li, M., Tao, J., Li, S., et al. (2026) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2026.110470 · Cited by 1 · see citing works
Moisander, P. H., & Ochiai, M. (2020) · Microbiology Resource Announcements · doi:10.1128/mra.01086-19 · Cited by 1 · see citing works
“The sorted cells directly underwent whole-genome amplification as described previously (REPLI-g midikit; Qiagen, USA) (3).”
MethodBioinformatic investigations in marine microbial ecology
Heller, P. (2014) · eScholarship (California Digital Library)
Fang, J., Zuo, S., Zheng, S., & Fang, S. (2026) · Applied Soil Ecology · doi:10.1016/j.apsoil.2026.107134
- Authors
- Bench, S. R., Ilikchyan, I. N., Tripp, H. J., & Zehr, J. P.
- Affiliations
- University of California, Santa Cruz (US)
- Corresponding author
- Zehr, Jonathan P.
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2011
- Volume
- 2
- Pages
- 261-261
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC3247675
- OpenAlex
- W2019431867
- Cited by
- 43
- References
- 72
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 4 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 3 · 2013: 5 · 2012: 3
- FWCI
- 1.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (0424599)
- Gordon and Betty Moore Foundation (EF0424599)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- Crocosphaera watsonii, genome rearrangement, transposase, exopolysaccharide biosynthesis, phenotypic diversity, nitrogen-fixing cyanobacteria, marine phytoplankton, strain divergence
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