Colonies of the Marine Cyanobacterium Optimize Dust Utilization by Selective Collection and Retention of Nutrient-rich Particles

Overview

Journal iScience

Publisher Cell Press

Date 2022 Jan 10

PMID 35005537

Authors

Siyuan Wang

Coco Koedooder

Futing Zhang

Nivi Kessler

Meri Eichner

Dalin Shi

Yeala Shaked

Affiliations

Soon will be listed here.

Abstract

, a globally important, N-fixing, and colony-forming cyanobacterium, employs multiple pathways for acquiring nutrients from air-borne dust, including active dust collection. Once concentrated within the colony core, dust can supply with nutrients. Recently, we reported a selectivity in particle collection enabling to center iron-rich minerals and optimize its nutrient utilization. In this follow-up study we examined if colonies select Phosphorus (P) minerals. We incubated 1,200 colonies from the Red Sea with P-free CaCO, P-coated CaCO, and dust, over an entire bloom season. These colonies preferably interacted, centered, and retained P-coated CaCO compared with P-free CaCO. In both studies, clearly favored dust over all other particles tested, whereas nutrient-free particles were barely collected or retained, indicating that the colonies sense the particle composition and preferably collect nutrient-rich particles. This unique ability contributes to 's current ecological success and may assist it to flourish in future warmer oceans.

Citing Articles

Recurrent association between colonies and calcifying amoebae.

Zhang F, Wang S, Visser A, Koedooder C, Eichner M, Anderson O ISME Commun. 2024; 4(1):ycae137.

PMID: 39564584 PMC: 11575492. DOI: 10.1093/ismeco/ycae137.

Single-colony MALDI mass spectrometry imaging reveals spatial differences in metabolite abundance between natural and cultured morphotypes.

Romanowicz K, Zhang F, Wang S, Velickovic D, Chu R, Shaked Y mSystems. 2024; 9(10):e0115224.

PMID: 39315778 PMC: 11501100. DOI: 10.1128/msystems.01152-24.

Phosphorus deficiency alleviates iron limitation in Synechocystis cyanobacteria through direct PhoB-mediated gene regulation.

Qiu G, Zheng W, Yang H, Wang Y, Qi X, Huang D Nat Commun. 2024; 15(1):4426.

PMID: 38789507 PMC: 11126600. DOI: 10.1038/s41467-024-48847-4.

Taxonomic distribution of metabolic functions in bacteria associated with consortia.

Koedooder C, Zhang F, Wang S, Basu S, Haley S, Tolic N mSystems. 2023; 8(6):e0074223.

PMID: 37916816 PMC: 10734445. DOI: 10.1128/msystems.00742-23.

Aerosol Nutrients and Their Biological Influence on the Northwest Pacific Ocean (NWPO) and Its Marginal Seas.

Guo C, Zhou Y, Zhou H, Su C, Kong L Biology (Basel). 2022; 11(6).

PMID: 35741363 PMC: 9219953. DOI: 10.3390/biology11060842.

References

Sanudo-Wilhelmy S, Tovar-Sanchez A, Fu F, Capone D, Carpenter E, Hutchins D . The impact of surface-adsorbed phosphorus on phytoplankton Redfield stoichiometry. Nature. 2004; 432(7019):897-901. DOI: 10.1038/nature03125. View

Capone D, Carpenter E . Nitrogen fixation in the marine environment. Science. 1982; 217(4565):1140-2. DOI: 10.1126/science.217.4565.1140. View

Orchard E, Webb E, Dyhrman S . Molecular analysis of the phosphorus starvation response in Trichodesmium spp. Environ Microbiol. 2009; 11(9):2400-11. DOI: 10.1111/j.1462-2920.2009.01968.x. View

Martiny A, Lomas M, Fu W, Boyd P, Chen Y, Cutter G . Biogeochemical controls of surface ocean phosphate. Sci Adv. 2019; 5(8):eaax0341. PMC: 6713502. DOI: 10.1126/sciadv.aax0341. View

Dyhrman S, Chappell P, Haley S, Moffett J, Orchard E, Waterbury J . Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature. 2006; 439(7072):68-71. DOI: 10.1038/nature04203. View

Bergman B, Sandh G, Lin S, Larsson J, Carpenter E . Trichodesmium--a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev. 2012; 37(3):286-302. PMC: 3655545. DOI: 10.1111/j.1574-6976.2012.00352.x. View

Zhang Z, Goldstein H, Reynolds R, Hu Y, Wang X, Zhu M . Phosphorus Speciation and Solubility in Aeolian Dust Deposited in the Interior American West. Environ Sci Technol. 2018; 52(5):2658-2667. DOI: 10.1021/acs.est.7b04729. View

Jickells T, An Z, Andersen K, Baker A, Bergametti G, Brooks N . Global iron connections between desert dust, ocean biogeochemistry, and climate. Science. 2005; 308(5718):67-71. DOI: 10.1126/science.1105959. View

Wu J, Sunda W, Boyle E, Karl D . Phosphate depletion in the western North Atlantic Ocean. Science. 2000; 289(5480):759-62. DOI: 10.1126/science.289.5480.759. View

10.

Polyviou D, Hitchcock A, Baylay A, Moore C, Bibby T . Phosphite utilization by the globally important marine diazotroph Trichodesmium. Environ Microbiol Rep. 2015; 7(6):824-30. DOI: 10.1111/1758-2229.12308. View

11.

Kessler N, Armoza-Zvuloni R, Wang S, Basu S, Weber P, Stuart R . Selective collection of iron-rich dust particles by natural Trichodesmium colonies. ISME J. 2019; 14(1):91-103. PMC: 6908701. DOI: 10.1038/s41396-019-0505-x. View

12.

Van Mooy B, Fredricks H, Pedler B, Dyhrman S, Karl D, Koblizek M . Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature. 2009; 458(7234):69-72. DOI: 10.1038/nature07659. View

13.

Tang W, Cerdan-Garcia E, Berthelot H, Polyviou D, Wang S, Baylay A . New insights into the distributions of nitrogen fixation and diazotrophs revealed by high-resolution sensing and sampling methods. ISME J. 2020; 14(10):2514-2526. PMC: 7490393. DOI: 10.1038/s41396-020-0703-6. View

14.

Basu S, Gledhill M, de Beer D, Prabhu Matondkar S, Shaked Y . Colonies of marine cyanobacteria interact with associated bacteria to acquire iron from dust. Commun Biol. 2019; 2:284. PMC: 6677733. DOI: 10.1038/s42003-019-0534-z. View

15.

Barkley A, Prospero J, Mahowald N, Hamilton D, Popendorf K, Oehlert A . African biomass burning is a substantial source of phosphorus deposition to the Amazon, Tropical Atlantic Ocean, and Southern Ocean. Proc Natl Acad Sci U S A. 2019; 116(33):16216-16221. PMC: 6697889. DOI: 10.1073/pnas.1906091116. View

16.

Mills M, Ridame C, Davey M, La Roche J, Geider R . Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature. 2004; 429(6989):292-4. DOI: 10.1038/nature02550. View

17.

Mackey K, Roberts K, Lomas M, Saito M, Post A, Paytan A . Enhanced solubility and ecological impact of atmospheric phosphorus deposition upon extended seawater exposure. Environ Sci Technol. 2012; 46(19):10438-46. DOI: 10.1021/es3007996. View

18.

Genga A, Siciliano T, Siciliano M, Aiello D, Tortorella C . Individual particle SEM-EDS analysis of atmospheric aerosols in rural, urban, and industrial sites of Central Italy. Environ Monit Assess. 2018; 190(8):456. DOI: 10.1007/s10661-018-6826-9. View

19.

Sanudo-Wilhelmy S, Kustka A, Gobler C, Hutchins D, Yang M, Lwiza K . Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature. 2001; 411(6833):66-9. DOI: 10.1038/35075041. View

20.

Thingstad T, Krom M, Mantoura R, Flaten G, Groom S, Herut B . Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science. 2005; 309(5737):1068-71. DOI: 10.1126/science.1112632. View