Abstract
Trichodesmium spp. are diazotrophic cyanobacteria that exist as single filaments (trichomes) and as macroscopic colonies of varying shapes formed by aggregating trichomes. The causes and dynamics of colony formation and disassociation are not yet elucidated. we demonstrate that limited availability of dissolved phosphorus (P) or iron (Fe) stimulated trichome mobility and induced colony formation in Trichodesmium erythraeum IMS101 cultures. The specific nutrient limitation differentially affected the rate of colony formation and morphology of the colonies. Fe starvation promoted rapid colony formation (10–48 h from depletion) while 5–7 days were required for colonies to form in P-depleted cultures. Video analyses confirmed that the probability of trichomes to cluster increased from 12 to 35% when transferred from nutrient replete to Fe-depleted conditions. Moreover, the probability for Fe-depleted aggregates to remain colonial increased to 50% from only 10% in nutrient replete cultures. These colonies were also characterized by stronger attachment forces between the trichomes. Enrichment of nutrient-depleted cultures with the limited nutrient-stimulated colony dissociation into single trichomes. We postulate that limited P and Fe availability enhance colony formation of Trichodesmium and primarily control the abundance and distribution of its different morphologies in the nutrient-limited surface ocean.
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References
Carpenter EJ, Subramaniam A, Capone DG. Biomass and primary productivity of the cyanobacterium Trichodesmium spp. in the tropical N Atlantic ocean. Deep Sea Res I. 2004;51:173–203.
Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ. Trichodesmium, a globally significant marine cyanobacterium. Science. 1997;276:1221–9.
Hynes AM, Webb EA, Doney SC, Waterbury JB. Comparison of cultured Trichodesmium (Cyanophyceae) with species characterized from the field. J Phycol. 2012;48:196–210.
Eichner MJ, Klawonn I, Wilson ST, Littmann S, Whitehouse MJ, Church MJ, et al. Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2. ISME J. 2017; 11:1305–17.
Rouco M, Haley ST, Dyhrman ST. Microbial diversity within the Trichodesmium holobiont. Environ Microbiol. 2016;18:5151–60.
Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, et al. Processes and patterns of oceanic nutrient limitation. Nat Geosci. 2013;6:701–10.
Dugdale RC, Menzel DW, Ryther J. Nitrogen fixation in the Sargasso Sea. Deep Res. 1961;7:297–300.
Carpenter E, Price C. Marine oscillatoria (Trichodesmium): explanation for aerobic nitrogen fixation without heterocysts. Science. 1976;191:1278–80.
Saino T, Hattori A. Aerobic nitrogen fixation by the marine non-heterocystous cyanobacterium Trichodesmium (Oscillatoria) spp.: Its protective mechanism against oxygen. Mar Biol. 1982;70:251–4.
Berman-Frank I, Lundgren P, Chen Y-B, Kupper H, Kolber Z, Bergman B, et al. Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science. 2001;294:1534–7.
Paerl HW. Spatial segregation of CO2 fixation in Trichodesmium spp.: linkage to N2 fixation potential. J Phycol. 1994;30:790–9.
Robson BJ, Baird M, Wild-Allen K. A physiological model for the marine cyanobacteria, Trichodesmium. In: Piantadosi J, Anderssen R, Boland J, editors. MODSIM2013, 20th International Congress on Modelling and Simulation. Ade laide: Modelling and Simulation Society of Australia and New Zealand; 2013. p. 1652–8.
Villareal TA, Carpenter EJ. Buoyancy regulation and the potential for vertical migration in the oceanic cyanobacterium Trichodesmium. Microb Ecol. 2003;45:1–10.
White AE, Spitz YH, Letelier RM. Modeling carbohydrate ballasting by Trichodesmium spp. Mar Ecol Prog Ser. 2006;323:35–45.
Letelier RM, Karl DM. Trichodesmium spp. physiology and nutrient fluxes in the North Pacific subtropical gyre. Aquat Microb Ecol. 1998;15:265–76.
Walsby AE. The properties and buoyancy-providing role of gas vacuoles in Trichodesmium Ehrenberg. Br Phycol J. 1978;13:103–16.
Rubin M, Berman-Frank I, Shaked Y. Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium. Nat Geosci. 2011;4:529–34.
Rueter JG, Hutchins DA, Smith RW, Unsworth NL. Iron nutrition of Trichodesmium. In: Carpenter EJ, Capone DG, Rueter JG, editors. Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs. Dordrecht: Springer Netherlands; 1992. p. 289–306.
Van-Mooy BAS, Hmelo LR, Sofen LE, Campagna SR, May AL, Dyhrman ST, et al. Quorum sensing control of phosphorus acquisition in Trichodesmium consortia. ISME J. 2011;6:422–9.
Chen Y-BB, Zehr JP, Mellon M. Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp IMS 101 in defined media: evidence for a circadian rhythm. J Phycol. 1996;32:916–23.
Bell PRF, Uwins PJR, Elmetri I, Phillips JA, Fu FX, Yago AJE. Laboratory culture studies of Trichodesmium isolated from the Great Barrier Reef lagoon, Australia. Hydrobiologia. 2005;532:9–21.
Ohki K, Fujita Y. Aerobic nitrogenase activity measured as acetylene reduction in the marine non-heterocystous cyanobacterium Trichodesmium spp. grown under artificial conditions. Mar Biol. 1988;98:111–4.
Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG. The demise of the marine cyanobacterium, Trichodesmium., via an autocatalyzed cell death pathway. Limnol Oceanogr. 2004;49:997–1005.
Davis CS. Transatlantic abundance of the N2-fixing colonial cyanobacterium Trichodesmium. Science. 2006;312:1517–20.
Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol Oceanogr. 2001;46:1249–60.
Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, et al. Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature. 2001;411:66–69.
Snow JT, Schlosser C, Woodward EMS, Mills MM, Achterberg EP, Mahaffey C, et al. Environmental controls on the biogeography of diazotrophy and Trichodesmium in the Atlantic Ocean. Glob Biogeochem Cycles. 2015;29:865–84.
Chappell PD, Webb EA. A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environ Microbiol. 2010;12:13–27.
Bar-Zeev E, Avishay I, Bidle KD, Berman-Frank I. Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export. ISME J. 2013;7:2340–8.
Gamliel H, Gurfel D, Leizerowitz R, Polliack A. Air-drying of human leucocytes for scanning electron microscopy using the GTGO procedure. J Microsc. 1983;131:87–95.
Stihl A, Sommer U, Post AF. Alkaline phosphatase activities among populations of the colony-forming diazotrophic cyanobacterium Trichodesmium spp. (cyanobacteria) in the Red Sea. J Phycol. 2001;37:310–7.
Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, et al. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature. 2006;439:68–71.
Polyviou D, Hitchcock A, Baylay AJ, Moore CM, Bibby TS. Phosphite utilization by the globally important marine diazotroph Trichodesmium. Environ Microbiol Rep. 2015;7:824–30.
Spungin D, Berman-Frank I, Levitan O. Trichodesmium’s strategies to alleviate phosphorus limitation in the future acidified oceans. Environ Microbiol. 2014;16:1935–47.
Berman-Frank I, Rosenberg G, Levitan O, Haramaty L, Mari X. Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ Microbiol. 2007;9:1415–22.
Sand-Jensen K. Ecophysiology of gelatinous Nostoc colonies: unprecedented slow growth and survival in resource-poor and harsh environments. Ann Bot. 2014;114:17–33.
Zhang M, Shi X, Yu Y, Kong F. The acclimative changes in photochemistry after colony formation of the cyanobacteria Microcystis aeruginosa. J Phycol. 2011;47:524–32.
Sellner KG. Physiology, ecology, and toxic properties of marine cyanobacteria blooms. Limnol Oceanogr. 1997;42:1089–104.
Dubey GP, Ben-Yehuda S. Intercellular nanotubes mediate bacterial communication. Cell. 2011;144:590–600.
Sure S, Ackland ML, Torriero AAJ, Adholeya A, Kochar M. Microbial nanowires: an electrifying tale. Microbiology. 2016;162:2017–28.
Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc Natl Acad Sci USA. 2014;111:12883–8.
Remis JP, Wei D, Gorur A, Zemla M, Haraga J, Allen S, et al. Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol. 2014;16:598–610.
Sheridan CC. The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey. J Plankton Res. 2002;24:913–22.
Sure S, Torriero AAJ, Gaur A, Li LH, Chen Y, Tripathi C, et al. Inquisition of Microcystis aeruginosa and Synechocystis nanowires: characterization and modelling. Antonie Van Leeuwenhoek. 2015;108:1213–25.
Sure S, Torriero AAJ, Gaur A, Li LH, Chen Y, Tripathi C, et al. Identification and topographical characterisation of microbial nanowires in Nostoc punctiforme. Antonie Van Leeuwenhoek. 2016;109:475–80.
Kupper H, Setlik I, Seibert S, Prasil O, Setlikova E, Strittmatter M, et al. Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. New Phytol. 2008;179:784–98.
Berman-Frank I, Quigg A, Finkel ZV, Irwin AJ, Haramaty L. Nitrogen-fixation strategies and Fe requirements in cyanobacteria. Limnol Oceanogr. 2007;52:2260–9.
Schoffman H, Lis H, Shaked Y, Keren N. Iron–nutrient interactions within phytoplankton. Front Plant Sci. 2016;7:1–12.
Jickells TD. Global iron connections between desert dust, ocean biogeochemistry, and climate. Science. 2005;308:67–71.
Guieu C, Aumont O, Paytan A, Bopp L, Law CS, Mahowald N, et al. The significance of the episodic nature of atmospheric deposition to low nutrient low chlorophyll regions. Glob Biogeochem Cycles. 2014;28:1179–98.
Roe KL, Barbeau K, Mann EL, Haygood MG. Acquisition of iron by Trichodesmium and associated bacteria in culture. Environ Microbiol. 2012;14:1681–95.
Dyhrman ST, Benitez-Nelson CR, Orchard ED, Haley ST, Pellechia PJ. A microbial source of phosphonates in oligotrophic marine systems. Nat Geosci. 2009;2:696–9.
Orchard ED, Webb EA, Dyhrman ST. Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol. 2009;11:2400–11.
Sohm J, Capone D. Phosphorus dynamics of the tropical and subtropical North Atlantic: Trichodesmium spp. versus bulk plankton. Mar Ecol Prog Ser. 2006;317:21–28.
White AE, Karl DM, Björkman KM, Beversdorf LJ, Letelier RM, White AE, et al. Phosphonate metabolism by Trichodesmium IMS101 and the production of greenhouse gases. Limnol Oceanogr. 2010;55:1768–78.
Orchard ED, Benitez-Nelson CR, Pellechia PJ, Lomas MW, Dyhrman ST. Polyphosphate in Trichodesmium from the low-phosphorus Sargasso Sea. Limnol Oceanogr. 2010;55:2161–9.
Romans KM, Carpenter EJ, Bergman B. Buoyancy regulation in the colonial diazotrophic cyanobacterium Trichodesmium tenue: ultrastructure and storage of carbohydrate, polyphosphate, and nitrogen. J Phycol. 1994;30:935–42.
White AE, Spitz YH, Karl DM, Letelier RM. Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol Oceanogr. 2006;51:1777–90.
Beardall J, Allen D, Bragg J, Finkel ZV, Flynn KJ, Quigg A, et al. Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytol. 2009;181:295–309.
Hewson I, Poretsky RS, Dyhrman ST, Zielinski B, White AE, Tripp HJ, et al. Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean. ISME J. 2009;3:1286–1300.
Hmelo L, Van Mooy B, Mincer T. Characterization of bacterial epibionts on the cyanobacterium Trichodesmium. Aquat Microb Ecol. 2012;67:1–14.
Momper LM, Reese BK, Carvalho G, Lee P, Webb EA. A novel cohabitation between two diazotrophic cyanobacteria in the oligotrophic ocean. ISME J. 2015;9:882–93.
Orchard ED, Ammerman JW, Lomas MW, Dyhrman ST. Dissolved inorganic and organic phosphorus uptake in Trichodesmium and the microbial community: The importance of phosphorus ester in the Sargasso Sea. Limnol Oceanogr. 2010;55:1390–9.
Lee MD, Walworth NG, McParland EL, Fu F-X, Mincer TJ, Levine NM, et al. The Trichodesmium consortium: conserved heterotrophic co-occurrence and genomic signatures of potential interactions. ISME J. 2017;11:1813–24.
Ma J, Brookes JD, Qin B, Paerl HW, Gao G, Wu P, et al. Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in Lake Taihu, China. Harmful Algae. 2014;31:136–42.
Callieri C, Lami A, Bertoni R. Microcolony formation by single-cell Synechococcus strains as a fast response to UV radiation. Appl Environ Microbiol. 2011;77:7533–40.
Yang H, Cai Y, Xia M, Wang X, Shi L, Li P, et al. Role of cell hydrophobicity on colony formation in Microcystis (cyanobacteria). Int Rev Hydrobiol. 2011;96:141–8.
Gan N, Xiao Y, Zhu L, Wu Z, Liu J, Hu C, et al. The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ Microbiol. 2012;14:730–42.
Van Donk E, Ianora A, Vos M. Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia. 2011;668:3–19.
Zhen Y, Kong F. Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas spp. J Limnol. 2012;71:61–66.
Callieri C, Amalfitano S, Corno G, Bertoni R. Grazing-induced Synechococcus microcolony formation: experimental insights from two freshwater phylotypes. FEMS Microbiol Ecol. 2016;92:1–10.
Oliver RL. Floating and sinking in gas-vacuolate cyanobacteria. J Phycol. 1994;30:161–73.
Holl CM, Villareal Ta, Payne CD, Clayton TD, Hart C, Montoya JP. Trichodesmium in the western Gulf of Mexico: 15N 2 -fixation and natural abundance stable isotopic evidence. Limnol Oceanogr. 2007;52:2249–59.
Villareal TA. Abundance and photosynthetic characteristics of Trichodesmium spp. along the Atlantic Barrier Reef at Carrie Bow Cay, Belize. Mar Ecol. 1995;16:259–71.
Olson EM, McGillicuddy DJ, Flierl GR, Davis CS, Dyhrman ST, Waterbury JB. Mesoscale eddies and Trichodesmium spp. distributions in the southwestern North Atlantic. J Geophys Res Ocean. 2015;120:4129–50.
Carpenter EJ, Romans KM. Major role of the cyanobacterium Trichodesmium in nutrient cycling in the North Atlantic. Ocean Sci. 1991;254:1356–8.
Mulholland MR, Floge S, Carpenter EJ, Capone DG. Phosphorus dynamics in cultures and natural population of Trichodesmim spp. Mar Ecol Prog Ser. 2002;239:45–55.
Orcutt KM, Gundersen K, Ammerman JW. Intense ectoenzyme activities associated with Trichodesmium colonies in the Sargasso Sea. Mar Ecol Prog Ser. 2013;478:101–13.
Letelier RM, Karl DM. Role of Trichodesmium spp. in the productivity of the subtropical North Pacific Ocean. Mar Ecol Prog Ser. 1996;133:263–73.
Rodier M, Le Borgne R. Population dynamics and environmental conditions affecting Trichodesmium spp. (filamentous cyanobacteria) blooms in the south–west lagoon of New Caledonia. J Exp Mar Bio Ecol. 2008;358:20–32.
Acknowledgements
We thank Dr. Avi Jacob of the light microscopy unit and Dr. Yaakov Langsam of the E-SEM unit at Bar Ilan University for their generous help and support in preparation and analyses. AB is thankful for partial support from the Israel Science Foundation Grant No. 373/16, and the Roy J. Zuckerberg Career Development Chair for Water Research for partial support. Funding for IBF was via the Schulich Ocean Studies Centre Initiative at Dalhousie University, and a collaborative grant from MOST Israel and the High Council for Science and Technology (HCST), France. This work is in partial fulfillment of the requirements for a PhD thesis for YT and an MSc thesis for LM at Bar Ilan University. Support for YT was provided with a student fellowship from the Mediterranean Sea Research Center of Israel (MERCI).
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Tzubari, Y., Magnezi, L., Be’er, A. et al. Iron and phosphorus deprivation induce sociality in the marine bloom-forming cyanobacterium Trichodesmium. ISME J 12, 1682–1693 (2018). https://doi.org/10.1038/s41396-018-0073-5
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DOI: https://doi.org/10.1038/s41396-018-0073-5
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