Abstract
The assimilation of organic nutrients by autotrophs, a form of mixotrophy, has been demonstrated in the globally abundant marine picocyanobacterial genera Prochlorococcus and Synechococcus. However, the range of compounds used and the distribution of organic compound uptake genes within picocyanobacteria are unknown. Here we analyze genomic and metagenomic data from around the world to determine the extent and distribution of mixotrophy in these phototrophs. Analysis of 49 Prochlorococcus and 18 Synechococcus isolate genomes reveals that all have the transporters necessary to take up amino acids, peptides and sugars. However, the number and type of transporters and associated catabolic genes differ between different phylogenetic groups, with low-light IV Prochlorococcus, and 5.1B, 5.2 and 5.3 Synechococcus strains having the largest number. Metagenomic data from 68 stations from the Tara Oceans expedition indicate that the genetic potential for mixotrophy in picocyanobacteria is globally distributed and differs between clades. Phylogenetic analyses indicate gradual organic nutrient transporter gene loss from the low-light IV to the high-light II Prochlorococcus. The phylogenetic differences in genetic capacity for mixotrophy, combined with the ubiquity of picocyanobacterial organic compound uptake genes suggests that mixotrophy has a more central role in picocyanobacterial ecology than was previously thought.
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References
Ahlgren NA, Rocap G . (2012). Diversity and distribution of marine Synechococcus: Multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Front Microbiol 3: 1–24.
Ahlgren NA, Rocap G, Chisholm SW . (2006). Measurement of Prochlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies. Environ Microbiol 8: 441–454.
Behrenfeld MJ, Falkowski PG . (1997). Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol Oceanogr 42: 1–20.
Béjà O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP et al. (2000). Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science (80-) 289: 1902–1906.
Béjà O, Spudich EN, Spudich JL, Leclerc M, DeLong EF . (2001). Proteorhodopsin phototrophy in the ocean. Nature 411: 786–789.
Campbell BJ, Waidner LA, Cottrell MT, Kirchman DL . (2008). Abundant proteorhodopsin genes in the North Atlantic Ocean. Environ Microbiol 10: 99–109.
Chen TH, Chen TL, Hung LM, Huang TC . (1991). Circadian rhythm in amino acid uptake by Synechococcus RF-1. Plant Physiol 97: 55–59.
Church MJ, Ducklow HW, Karl DM . (2004). Light dependence of [ 3 H ] leucine incorporation in the oligotrophic North Pacific Ocean light dependence of [ 3 H ] leucine incorporation in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 70: 4079–4087.
Cubillos-Ruiz AF, Thompson JW, Becker JW, Chisholm SW, Shi Y, Van der Donk WA et al. (2015). Ecology and evolution of lanthipeptides in marine picocyanobacteria. (Doctoral dissertation). Retrieved from DSpace MIT Thesis Database.
Cullen JJ . (2015). Subsurface chlorophyll maximum layers: enduring enigma or mystery solved? Ann Rev Mar Sci 7: 207–239.
Cunningham CW, Omland KE, Oakley TH . (1998). Reconstructing ancestral character states: a critical reappraisal. Trends Ecol Evol 13: 361–366.
Dandekar T, Snel B, Huynen M, Bork P . (1998). Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23: 324–328.
Dauvillée D, Kinderf IS, Li Z, Kosar-Hashemi B, Samuel MS, Rampling L et al. (2005). Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187: 1465–1473.
Dufresne A, Ostrowski M, Scanlan DJ, Garczarek L, Mazard S, Palenik B et al. (2008). Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Genome Biol 9: R90.
Edgar RC . (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461.
Evans C, Gómez-Pereira PR, Martin AP, Scanlan DJ, Zubkov MV . (2015). Photoheterotrophy of bacterioplankton is ubiquitous in the surface oligotrophic ocean. Prog Oceanogr 135: 139–145.
Ferris MJ, Palenik B . (1998). Niche adaptation in ocean cyanobacteria. Nature 396: 226–228.
Finkel OM, Béjà O, Belkin S . (2013). Global abundance of microbial rhodopsins. ISME J 7: 448–451.
Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N et al. (2013). Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci USA 110: 9824–9829.
Gómez-Baena G, López-Lozano A, Gil-Martínez J, Lucena JM, Diez J, Candau P et al. (2008). Glucose uptake and its effect on gene expression in Prochlorococcus. PLoS One 3: e3416.
Gómez-Pereira PR, Hartmann M, Grob C, Tarran GA, Martin AP, Fuchs BM et al. (2013). Comparable light stimulation of organic nutrient uptake by SAR11 and Prochlorococcus in the North Atlantic subtropical gyre. ISME J 7: 603–614.
Hancock REW, Carey AM . (1980). Protein D1: a glucose-inducible, pore-forming protein from the outer membrane of Pseudomonas aeruginosa. FEMS Microbiol Lett 8: 105–109.
Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ et al. (2012). Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc Natl Acad Sci USA 109: 5756–5760.
Hingamp P, Grimsley N, Acinas SG, Clerissi C, Subirana L, Poulain J et al. (2013). Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME J 7: 1678–1695.
Huang S, Wilhelm SW, Harvey HR, Taylor K, Jiao N, Chen F . (2012). Novel lineages of Prochlorococcus and Synechococcus in the global oceans. ISME J 6: 285–297.
Hurwitz BL, Sullivan MB . (2013). The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One 8: e57355.
Huynen M, Snel B, Lathe W, Bork P . (2000). Predicting protein function by genomic context: quantitative evaluation and qualitative inferences. Genome Res 10: 1204–1210.
Jeanningros R, Creuzet-Sigal N, Frixon C, Cattaneo J . (1976). Purification and properties of a debranching enzyme from Escherichia coli. Biochim Biophys Acta 438: 186–199.
Jiao N, Zhang Y, Zeng Y, Hong N, Liu R, Chen F et al. (2007). Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ Microbiol 9: 3091–3099.
Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW . (2006). Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science (80-) 311: 1737–1740.
Jones RI . (2000). Mixotrophy in planktonic protists: an overview. Freshw Biol 45: 219–226.
Joset-Espardellier F, Astier C, Evans EH, Carr NG . (1978). Cyanobacteria grown under photoautotrophic, photoheterotrophic, and heterotrophic regimes: sugar metabolism and carbon dioxide fixation. FEMS Microbiol Lett 4: 261–264.
Kaiser K, Benner R . (2008). Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol Oceanogr 53: 99–112.
Karimpour-Fard A, Leach SM, Gill RT, Hunter LE . (2008). Predicting protein linkages in bacteria: which method is best depends on task. BMC Bioinformatics 9: 397.
Karsenti E, Acinas SG, Bork P, Bowler C, De Vargas C, Raes J et al. (2011). A holistic approach to marine eco-systems biology. PLoS Biol 9: e1001177.
Keil R, Kirchman D . (1999). Utilization of dissolved protein and amino acids in the northern Sargasso Sea. Aquat Microb Ecol 18: 293–300.
Kelly L, Huang KH, Ding H, Chisholm SW . (2012). ProPortal: a resource for integrated systems biology of Prochlorococcus and its phage. Nucleic Acids Res 40: 632–640.
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.
Kirchman D, Stegman M, Nikrad M, Cottrell M . (2014). Abundance, size, and activity of aerobic anoxygenic phototrophic bacteria in coastal waters of the West Antarctic Peninsula. Aquat Microb Ecol 73: 41–49.
Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, Vandover CL et al. (1999). Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292: 2492–2495.
Kultima JR, Sunagawa S, Li JH, Chen WN, Chen H, Mende DR et al. (2012). MOCAT: a metagenomics assembly and gene prediction toolkit. PLoS One 7: e47656.
Lahmi R, Sendersky E, Perelman A, Hagemann M, Forchhammer K, Schwarz R . (2006). Alanine dehydrogenase activity is required for adequate progression of phycobilisome degradation during nitrogen starvation in Synechococcus elongatus PCC 7942. J Bacteriol 188: 5258–5265.
Lavin P, González B, Santibáñez JF, Scanlan DJ, Ulloa O . (2010). Novel lineages of Prochlorococcus thrive within the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol Rep 2: 728–738.
Li B, Sher D, Kelly L, Shi Y, Huang K, Knerr PJ . (2010). Catalytic promiscuity in the biosynthesis of cyclic peptide secondary metabolites in planktonic marine cyanobacteria. Proc Natl Acad Sci USA 107: 10430–10435.
Logares R, Sunagawa S, Salazar G, Cornejo-Castillo FM, Ferrera I, Sarmento H et al. (2014). Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16: 2659–2671.
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.
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.
Martiny AC, Tai APK, Veneziano D, Primeau F, Chisholm SW . (2009). Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ Microbiol 11: 823–832.
Mary I, Garczarek L, Tarran GA, Kolowrat C, Terry MJ, Scanlan DJ et al. (2008). Diel rhythmicity in amino acid uptake by Prochlorococcus. Environ Microbiol 10: 2124–2131.
Michelou VK, Cottrell MT, Kirchman DL, David L . (2007). Light-stimulated bacterial production and amino acid assimilation by cyanobacteria and other microbes in the North Atlantic ocean. Appl Environ Microbiol 73: 5539–5546.
Moore LR, Chisholm SW . (1999). Photophysiology of the marine Ecotypic cyanobacterium Prochlorococcus: differences among cultured isolates. Limnol Oceanogr 44: 628–638.
Moore LR, Rocap G, Chisholm SW . (1998). Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464–467.
Mühling M, Fuller NJ, Millard A, Somerfield PJ, Marie D, Wilson WH et al. (2005). Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ Microbiol 7: 499–508.
Mühling M, Fuller NJ, Somerfield PJ, Post AF, Wilson WH, Scanlan DJ et al. (2006). High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length polymorphism. Aquat Microb Ecol 45: 263–275.
Muñoz-Marín MDC, Luque I, Zubkov MV, Hill PG, Diez J, García-Fernández JM . (2013). Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean. Proc Natl Acad Sci USA 110: 8597–8602.
Paerl HW . (1991). Ecophysiological and trophic implications of light-stimulated amino acid utilization in marine picoplankton. Appl Environ Microbiol 57: 473–479.
Palenik B . (1994). Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis. Appl Environ Microbiol 60: 3212–3219.
Palovaara J, Akram N, Baltar F, Bunse C, Forsberg J, Pedrós-Alió C et al. (2014). Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria. Proc Natl Acad Sci USA 111: 1–9.
Partensky F, Garczarek L, Hess WR, Vaulot D . (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106–127.
Partensky F, Hess WR, Vaulot D, Garczarek L . (2010). Prochlorococcus: advantages and limits of minimalism. Ann Rev Mar Sci 2: 305–331.
Perez RC, Matin A . (1980). Growth of Thiobacillus novellus on mixed substrates (Mixotrophic growth). J Bacteriol 142: 633–638.
Pesant S, Not F, Picheral M, Kandels-Lewis S, Le Bescot N, Gorsky G et al. (2015). Open science resources for the discovery and analysis of Tara Oceans data. Open Sci Resour Discov Anal Tara Ocean data Sci Data 2: 150023.
Raymond J, Blankenship RE . (2004). The evolutionary development of the protein complement of Photosystem 2. Biochim Biophys Acta - Bioenerg 1655: 133–139.
Rippka R . (1972). Photoheterotrophy and chemoheterotrophy among unicellular blue-green algae. Arch Mikrobiol 87: 93–98.
Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA et al. (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042–1047.
Rogozin IB, Makarova KS, Wolf YI, Koonin EV . (2004). Computational approaches for the analysis of gene neighbourhoods in prokaryotic genomes. Brief Bioinform 5: 131–149.
Rothhaupt KO . (1996a). Laboratory experiments with a mixotrophic chrysophyte and obligately phago- trophic and phototrophic competitors. Ecology 77: 716–724.
Rothhaupt KO . (1996b). Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte Ochromonas SP. Ecology 77: 706–715.
Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S et al. (2007). The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5: e77.
Sabehi G, Loy A, Jung KH, Partha R, Spudich JL, Isaacson T et al. (2005). New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol 3: e273.
Saier MH Jr, Tran CV, Barabote RD . (2006). TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 34: D181–D186.
Saravolac EG, Taylor NF, Benz R, Hancock REW . (1991). Purification of glucose-inducible outer membrane protein OprB of Pseudomonas putida and reconstitution of glucose-specific pores. J Bacteriol 173: 4970–4976.
Schlitzer R . (2002). Interactive analysis and visualization of geoscience data with Ocean Data View. Comput Geosci 28: 1211–1218.
Sieracki ME, Gilg IC, Thier EC, Poulton NJ, Goericke R . (2006). Distribution of planktonic aerobic anoxygenic photoheterotrophic bacteria in the northwest Atlantic. Limnol Oceanogr 51: 38–46.
Sohm JA, Ahlgren NA, Thomson ZJ, Williams C, Moffett JW, Saito MA et al. (2015). Co-occurring Synechococcus ecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron. ISME J 10: 1–13.
Stamatakis A . (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
Sun Z, Blanchard JL . (2014). Strong genome-wide selection early in the evolution of Prochlorococcus Resulted in a reduced genome through the loss of a large number of small effect genes. PLoS One 9: e88837.
Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G et al. (2015). Structure and function of the global ocean microbiome. Science (80-) 348: 1–10.
Suzuki E, Umeda K, Nihei S, Moriya K, Ohkawa H, Fujiwara S et al. (2007). Role of the GlgX protein in glycogen metabolism of the cyanobacterium, Synechococcus elongatus PCC 7942. Biochim Biophys Acta 1770: 763–773.
Team RDC. (2012) R: A Language and Environment for Statistical Computing.
Thompson JW . (2015) Prochlorococcus: life in light. (Doctoral dissertation). Retrieved from DSpace MIT Thesis Database.
Vila-Costa M, Simó R, Harada H, Gasol JM, Slezak D, Kiene RP . (2006). Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314: 652–654.
West NJ, Scanlan DJ . (1999). Niche-partitioning of Prochlorococcus populations in a stratified water column in the eastern North Atlantic Ocean. Appl Environ Microbiol 65: 2585–2591.
West NJ, Schonhuber WA, Fuller NJ, Amann RI, Rippka R, Post AF et al. (2001). Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides. Microbiology 147: 1731–1744.
Ye Y, Choi J-H, Tang H . (2011). RAPSearch: a fast protein similarity search tool for short reads. BMC Bioinformatics 12: 159.
Yelton AP, Thomas BC, Simmons SL, Wilmes P, Zemla A, Thelen MP et al. (2011). A semi-quantitative, synteny-based method to improve functional predictions for hypothetical and poorly annotated bacterial and archaeal genes. PLoS Comput Biol 7: e1002230.
Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K et al. (2007). The Sorcerer II global ocean sampling expedition: expanding the universe of protein families. PLoS Biol 5: 0432–0466.
Zinser ER, Coe A, Johnson ZI, Martiny AC, Fuller NJ, Scanlan DJ et al. (2006). Prochlorococcus ecotype abundances in the North Atlantic Ocean as revealed by an improved quantitative PCR method. Appl Environ Microbiol 72: 723–732.
Zinser ER, Johnson ZI, Coe A, Karaca E, Veneziano D, Chisholm SW . (2007). Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean. Limnol Oceanogr 52: 2205–2220.
Zubkov MV, Fuchs BM, Tarran GA, Burkill PH, Amann R . (2003). High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol 69: 1299–1304.
Zubkov MV, Tarran GA, Fuchs BM . (2004). Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropical gyre. FEMS Microbiol Ecol 50: 153–161.
Zubkov MV . (2009). Photoheterotrophy in marine prokaryotes. J Plankton Res 31: 933–938.
Zubkov MV, Tarran GA, Mary I, Fuchs BM . (2008). Differential microbial uptake of dissolved amino acids and amino sugars in surface waters of the Atlantic Ocean. J Plankton Res 30: 211–220.
Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D et al. (2008). Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147–161.
Acknowledgements
We thank the US National Science Foundation OCE postdoctoral research fellowship program and the Fulbright Commission, Spain for supporting APY. The work was also supported in part by the European Molecular Biology Laboratory, grants to SWC from the Gordon and Betty Moore Foundation (grant GBMF495) the National Science Foundation (grants OCE-1356460 and DBI-0424599), grants from the Simons Foundation (grant 337262), the Spanish Ministry of Science and Innovation grant to SGA, CGL2011-26848/BOS MicroOcean PANGENOMICS and U FP7-OCEAN.2011-2. Micro3B Marine Microbial Biodiversity, the Bioinformatics and Biotechnology Large Collaborative grant 287589 and is a contribution of the Simons Collaboration on Ocean Processes and Ecology (SCOPE). We are indebted to the scientists and crew of the Tara Oceans expedition.
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Yelton, A., Acinas, S., Sunagawa, S. et al. Global genetic capacity for mixotrophy in marine picocyanobacteria. ISME J 10, 2946–2957 (2016). https://doi.org/10.1038/ismej.2016.64
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DOI: https://doi.org/10.1038/ismej.2016.64
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