Abstract
Interactions between marine microorganisms may determine the dynamics of microbial communities. Here, we show that two strains of the globally abundant marine cyanobacterium Prochlorococcus, MED4 and MIT9313, which belong to two different ecotypes, differ markedly in their response to co-culture with a marine heterotrophic bacterium, Alteromonas macleodii strain HOT1A3. HOT1A3 enhanced the growth of MIT9313 at low cell densities, yet inhibited it at a higher concentration, whereas it had no effect on MED4 growth. The early transcriptomic responses of Prochlorococcus cells after 20 h in co-culture showed no evidence of nutrient starvation, whereas the expression of genes involved in photosynthesis, protein synthesis and stress responses typically decreased in MED4 and increased in MIT313. Differential expression of genes involved in outer membrane modification, efflux transporters and, in MIT9313, lanthipeptides (prochlorosins) suggests that Prochlorococcus mount a specific response to the presence of the heterotroph in the cultures. Intriguingly, many of the differentially-expressed genes encoded short proteins, including two new families of co-culture responsive genes: CCRG-1, which is found across the Prochlorococcus lineage and CCRG-2, which contains a sequence motif involved in the export of prochlorosins and other bacteriocin-like peptides, and are indeed released from the cells into the media.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Amin SA, Green DH, Hart MC, Kupper FC, Sunda WG, Carrano CJ . (2009). Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proc Natl Acad Sci USA 106: 17071–17076.
Amin SA, Hmelo LR, Van Tol HM, Durham BP, Carlson LT, Heal KR et al. (2015). Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522: 98–101.
Arts IS, Gennaris A, Collet J-F . (2015). Reducing systems protecting the bacterial cell envelope from oxidative damage. FEBS Lett 589: 1559–1568.
Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D . (2011). Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 474: 604–608.
Azam F, Malfatti F . (2007). Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 966–U23.
Bar-Yosef Y, Sukenik A, Hadas O, Viner-Mozzini Y, Kaplan A . (2010). Enslavement in the water body by toxic Aphanizomenon ovalisporum, inducing alkaline phosphatase in phytoplanktons. Curr Biol 20: 1557–1561.
Bassler BL, Losick R . (2006). Bacterially speaking. Cell 125: 237–246.
Beliaev AS, Romine MF, Serres M, Bernstein HC, Linggi BE, Markillie LM et al. (2014). Inference of interactions in cyanobacterial-heterotrophic co-cultures via transcriptome sequencing. ISME J 8: 2243–2255.
Berg G, Shrager J, Van Dijken G, Mills M, Arrigo K, Grossman A . (2011). Responses of psbA, hli and ptox genes to changes in irradiance in marine Synechococcus and Prochlorococcus. Aquat Microb Ecol 65: 1–14.
Bertilsson S, Berglund O, Pullin MJ, Chisholm SW . (2005). Release of dissolved organic matter by Prochlorococcus. Vie Et Milieu-Life Environ 55: 225–231.
Biller SJ, Berube PM, Berta-Thompson JW, Kelly L, Roggensack SE, Awad L et al. (2014a). Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus. Sci Data 1: 140034.
Biller SJ, Schubotz F, Roggensack SE, Thompson AW, Summons RE, Chisholm SW . (2014b). Bacterial vesicles in marine ecosystems. Science 343: 183–186.
Blackburn N, Fenchel T, Mitchell J . (1998). Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282: 2254–2256.
Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke et al. (2000). A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407: 623–626.
Bouman HA, Ulloa O, Scanlan DJ, Zwirglmaier K, Li WK, Platt T et al. (2006). Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes. Science 312: 918–921.
Chatterjee C, Paul M, Xie L, Van Der Donk WA . (2005). Biosynthesis and mode of action of lantibiotics. Chem Rev 105: 633–684.
Christie-Oleza JA, Armengaud J, Guerin P, Scanlan DJ . (2015). Functional distinctness in the exoproteomes of marine Synechococcus. Environ Microbiol 17: 3781–3794.
Coleman ML, Chisholm SW . (2007). Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol 15: 398–407.
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG . (2005). Algae acquire vitamin B-12 through a symbiotic relationship with bacteria. Nature 438: 90–93.
Czaran TL, Hoekstra RF, Pagie L . (2002). Chemical warfare between microbes promotes biodiversity. Proc Natl Acad Sci USA 99: 786–790.
Diaz JM, Hansel CM, Voelker BM, Mendes CM, Andeer PF, Zhang T . (2013). Widespread production of extracellular superoxide by heterotrophic bacteria. Science 340: 1223–1226.
Dobáková M, Tichý M, Komenda J . (2007). Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 145: 1681–1691.
DuRand MD, Olson RJ, Chisholm SW . (2001). Phytoplankton population dynamics at the Bermuda Atlantic Time-series station in the Sargasso Sea. Deep Sea Res Part II 48: 1983–2003.
Dworkin J . (2014). The medium is the message: interspecies and interkingdom signaling by peptidoglycan and related bacterial glycans. Annu Rev Microbiol 68: 137–154.
Dwyer DJ, Kohanski MA, Collins JJ . (2009). Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 12: 482–489.
Eilers H, Pernthaler J, Glöckner FO, Amann R . (2000). Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66: 3044–3051.
Fadeev E, De Pascale F, Vezzi A, Hübner S, Aharonovich D, Sher D . (2016). Why close a bacterial genome? The plasmid of Alteromonas macleodii HOT1A3 is a vector for inter-specific transfer of a flexible genomic island. Front Microbiol 7: 248.
García-Martínez J, Acinas SG, Massana R, Rodríguez-Valera F . (2002). Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions. Environ Microbiol 4: 42–50.
Gebendorfer KM, Drazic A, Le Y, Gundlach J, Bepperling A, Kastenmüller A et al. (2012). Identification of a hypochlorite-specific transcription factor from Escherichia coli. J Biol Chem 287: 6892–6903.
Goecks J, Nekrutenko A, Taylor J . (2010). Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
Grishkevich V, Yanai I . (2014). Gene length and expression level shape genomic novelties. Genome Res 24: 1497–1503.
Heyn P, Kircher M, Dahl A, Kelso J, Tomancak P, Kalinka AT et al. (2014). The earliest transcribed zygotic genes are short, newly evolved, and different across species. Cell Rep 6: 285–292.
Hibbing ME, Fuqua C, Parsek MR, Peterson SB . (2009). Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15–25.
Ivars-Martinez E, Martin-Cuadrado A-B, D'auria G, Mira A, Ferriera S, Johnson J et al. (2008). Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J 2: 1194–1212.
Johnson ZI, Zinser ER, Coe A, Mcnulty NP, Woodward EM, Chisholm SW . (2006). Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311: 1737–1740.
Kettler GC, Martiny AC, Huang K, Zucker J, Coleman ML, Rodrigue S et al. (2007). Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 3: e231.
Langmead B, Trapnell C, Pop M, Salzberg SL . (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
Li B, Sher D, Kelly L, Shi Y, Huang K, Knerr PJ et al. (2010). Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. Proc Natl Acad Sci USA 107: 10430–10435.
Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T et al. (2007). Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449: 83–86.
Liu H, Huang RY, Chen J, Gross ML, Pakrasi HB . (2011). Psb27, a transiently associated protein, binds to the chlorophyll binding protein CP43 in photosystem II assembly intermediates. Proc Natl Acad Sci 108: 18536–18541.
Lopez-Perez M, Gonzaga A, Martin-Cuadrado AB, Onyshchenko O, Ghavidel A, Ghai R et al. (2012). Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep 2: 696.
Malfatti F, Azam F . (2009). Atomic force microscopy reveals microscale networks and possible symbioses among pelagic marine bacteria. Aquat Microb Ecol 58: 1–14.
Malmstrom RR, Coe A, Kettler GC, Martiny AC, Frias-Lopez J, Zinser ER et al. (2010). Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J 4: 1252–1264.
Malmstrom RR, Rodrigue S, Huang KH, Kelly L, Kern SE, Thompson A et al. (2012). Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis. ISME J 7: 184–198.
Martiny AC, Coleman ML, Chisholm SW . (2006). Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103: 12552–12557.
Mayali X, Azam F . (2004). Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51: 139–144.
McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR et al. (2010). Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA 107: 16420–16427.
McClure R, Balasubramanian D, Sun Y, Bobrovskyy M, Sumby P, Genco CA et al. (2013). Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res 41: e140.
Moore LR, Coe A, Zinser ER, Saito MA, Sullivan MB, Lindell D et al. (2007). Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr Methods 5: 353–362.
Morris JJ, Johnson ZI, Szul MJ, Keller M, Zinser ER . (2011). Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface. PLoS One 6: e16805.
Morris JJ, Kirkegaard R, Szul MJ, Johnson ZI, Zinser ER . (2008). Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by ‘helper’ heterotrophic bacteria. Appl Environ Microbiol 74: 4530–4534.
Morris JJ, Lenski RE, Zinser ER . (2012). The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3: pii: e00036-12.
Nakao M, Okamoto S, Kohara M, Fujishiro T, Fujisawa T, Sato S et al. (2010). CyanoBase: the cyanobacteria genome database update 2010. Nucleic Acids Res 38: D379–D381.
Ottesen EA, Young CR, Gifford SM, Eppley JM, Marin R, Schuster SC et al. (2014). Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345: 207–212.
Parks DH, Tyson GW, Hugenholtz P, Beiko RG . (2014). STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30: 3123–3124.
Partensky F, Garczarek L . (2010). Prochlorococcus: advantages and limits of minimalism. Annu Rev Mar Sci 2: 305–331.
Pasulka AL, Samo TJ, Landry MR . (2015). Grazer and viral impacts on microbial growth and mortality in the southern California Current Ecosystem. J Plankton Res 37: 320–336.
Paz-Yepes J, Brahamsha B, Palenik B . (2013). Role of a microcin-C-like biosynthetic gene cluster in allelopathic interactions in marine Synechococcus. Proc Natl Acad Sci USA 110: 12030–12035.
Pedler BE, Aluwihare LI, Azam F . (2014). Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean. Proc Natl Acad Sci 111: 7202–7207.
Pernthaler J . (2005). Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 3: 537–546.
Ribalet F, Swalwell J, Clayton S, Jiménez V, Sudek S, Lin Y et al. (2015). Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre. Proc Natl Acad Sci 112: 8008–8012.
Sacharz J, Bryan SJ, Yu J, Burroughs NJ, Spence EM, Nixon PJ et al. (2015). Sub-cellular location of FtsH proteases in the cyanobacterium Synechocystis sp. PCC 6803 suggests localised PSII repair zones in the thylakoid membranes. Mol Microbiol 96: 448–462.
Saito MA, Mcilvin MR, Moran DM, Goepfert TJ, Ditullio GR, Post AF et al. (2014). Multiple nutrient stresses at intersecting Pacific Ocean biomes detected by protein biomarkers. Science 345: 1173–1177.
Seymour JR, Simo R, Ahmed T, Stocker R . (2010). Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329: 342–345.
Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB . (2013). Rate-limiting steps in yeast protein translation. Cell 153: 1589–1601.
Sher D, Thompson JW, Kashtan N, Croal L, Chisholm SW . (2011). Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria. ISME J 5: 1125–1132.
Steglich C, Futschik M, Rector T, Steen R, Chisholm SW . (2006). Genome-wide analysis of light sensing in Prochlorococcus. J Bacteriol 188: 7796–7806.
Steglich C, Stazic D, Lott SC, Voigt K, Greengrass E, Lindell D et al. (2015). Dataset for metatranscriptome analysis of Prochlorococcus-rich marine picoplankton communities in the Gulf of Aqaba, Red Sea. Mar Genomics 19: 5–7.
Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF . (2008). Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci USA 105: 4209–4214.
Tai V, Paulsen IT, Phillippy K, Johnson DA, Palenik B . (2009). Whole-genome microarray analyses of Synechococcus-Vibrio interactions. Environ Microbiol 11: 2698–2709.
Thompson AW, Huang K, Saito MA, Chisholm SW . (2011). Transcriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability. ISME J 5: 1580–1594.
Tolonen AC, Aach J, Lindell D, Johnson ZI, Rector T, Steen R et al. (2006). Global gene expression of Prochlorococcus ecotypes in response to changes in nitrogen availability. Mol Syst Biol 2: 53.
Vaulot D, Marie D, Olson RJ, Chisholm SW . (1995). Growth of prochlorococcus, a photosynthetic prokaryote, in the equatorial pacific ocean. Science 268: 1480–1482.
Voigt K, Sharma CM, Mitschke J, Joke Lambrecht S, Vos B, Hess WR et al. (2014). Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity. ISME J 8: 2056–2068.
Waldbauer JR, Rodrigue S, Coleman ML, Chisholm SW . (2012). Transcriptome and proteome dynamics of a light-dark synchronized bacterial cell cycle. PLoS One 7: e43432.
Wang H, Fewer DP, Sivonen K . (2011). Genome mining demonstrates the widespread occurrence of gene clusters encoding bacteriocins in cyanobacteria. PLoS One 6: e22384.
Whidden CE, Dezeeuw KG, Zorz JK, Joy AP, Barnett DA, Johnson MS et al. (2014). Quantitative and functional characterization of the hyper-conserved protein of Prochlorococcus and marine Synechococcus. PLoS One 9: e109327.
Worden AZ, Binder BJ . (2003). Application of dilution experiments for measuring growth and mortality rates among Prochlorococcus and Synechococcus populations in oligotrophic environments. Aquat Microb Ecol 30: 159–174.
Zhaxybayeva O, Gogarten JP, Doolittle WF . (2007). A hyperconserved protein in Prochlorococcus and marine Synechococcus. FEMS Microbiol Lett 274: 30–34.
Acknowledgements
Parts of this research were conducted in the laboratory of Sallie Chisholm at MIT. We thank her and Allison Coe, Steve Biller and Andres Cubillos, as well as David Morgenstern, Assaf Malik, Ilia Burgsdorf, Dalit Rosenberg, Assaf Vardi, Eduard Fadeev and Noa Sher, for assistance and helpful comments on the manuscript. This study was supported by grant 2010183 from the United States-Israel Binational Science Foundation and Microbes-2-Model from the European Union FP7 Marie Curie Reintegration program (to DS). Partial support for the work was also provided by the following grants to Sallie Chisholm from the Gordon and Betty Moore Foundation (Grant award letters #495 and #495.01), the US National Science Foundation grant OCE-0425602 and the US Department of Energy grant DE-FG02-07ER64506.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies this paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Aharonovich, D., Sher, D. Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals. ISME J 10, 2892–2906 (2016). https://doi.org/10.1038/ismej.2016.70
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2016.70
This article is cited by
-
Phototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversity
The ISME Journal (2023)
-
Chemotaxis increases metabolic exchanges between marine picophytoplankton and heterotrophic bacteria
Nature Microbiology (2023)
-
A comparative whole-genome approach identifies bacterial traits for marine microbial interactions
Communications Biology (2022)
-
The initial inoculation ratio regulates bacterial coculture interactions and metabolic capacity
The ISME Journal (2021)
-
Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii
Scientific Reports (2020)
