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Aluminum-induced changes in the net carbon fixation and carbon decomposition of a nitrogen-fixing cyanobacterium Trichodesmium erythraeum

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Abstract

Recent studies suggest aluminum (Al) likely plays a role in the ocean carbon cycle by altering the biological carbon fixation and carbon decomposition of marine diatoms. However, it remains speculative whether Al has similar effects on other ecologically important phytoplankton groups such as the globally important nitrogen-fixing cyanobacterium, Trichodesmium. Here we report the influence of Al on carbon fixation and decomposition in non-axenic cultures of Trichodesmium erythraeum IMS101 (CCMP 1985). By using radiocarbon, and adding oceanic relevant amounts of dissolved Al (yielding concentrations of 40 and 200 nM) along with non-Al-amended controls, we investigated the changes in particulate organic carbon (POC) of Trichodesmium (> 2 μm, Trichodesmium POC), and free-living bacteria (0.2–2 μm, bacterial POC), and dissolved organic carbon (< 0.2 μm, DOC) over a 116-day growth period. The results showed that the rates of increase of POC in the declining growth phase of T. erythraeum were significantly higher (by 11–14%) in the Al-enriched treatments than in the control, and this Al-enhanced carbon fixation is consistent with previous observations on marine diatoms. On the other hand, unlike diatoms, the POC from T. erythraeum decomposed faster in the Al-enriched treatments during the first decay phase when bacterial POC and DOC increased along with the decomposition of Trichodesmium POC. Further addition of the same amounts of Al (again calculated to increase the Al concentration by 40 and 200 nM) was performed on day 71. This treatment was designed to mimic Al supply from sediment after the settling of Trichodesmium colonies to the ocean bottom. Following this second addition, the decomposition rate of both Trichodesmium POC and DOC slowed down by 20–27% and 31–62%, respectively, during the second decay phase, when DOC and bacterial POC decreased. The study suggests that Al fertilization in the surface ocean via dust deposition may increase the net carbon fixation and associated nitrogen fixation by Trichodesmium, and thus the supply of new nitrogen to the euphotic zone, whereas Al from sediment may decrease the decomposition rate of decaying Trichodesmium settled to the ocean bottom.

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Data availability

Data for this manuscript are available at the South China Sea Ocean Data Center, National Earth System Science Data Center, National Science & Technology Infrastructure of China (http://data.scsio.ac.cn/metaData-detail/1646764363844362240).

References

  • Ababou F-E, Le Moigne FAC, Grosso O, Guigue C, Nunige S, Camps M, Bonnet S (2023) Mechanistic understanding of diazotroph aggregation and sinking: “A rolling tank approach.” Limnol Oceanogr 68(3):666–677

    Article  Google Scholar 

  • Abramson L, Wirick S, Lee C, Jacobsen C, Brandes JA (2009) The use of soft X-ray spectromicroscopy to investigate the distribution and composition of organic matter in a diatom frustule and a biomimetic analog. Deep Sea Res II 56(18):1369–1380

    Article  Google Scholar 

  • Anderson RP, Tosca NJ, Cinque G, Frogley MD, Lekkas I, Akey A, Hughes GM, Bergmann KD, Knoll AH, Briggs DEG (2020) Aluminosilicate haloes preserve complex life approximately 800 million years ago. Interface Focus 10(4):20200011

    Article  Google Scholar 

  • Basu S, Shaked Y (2018) Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria. Limnol Oceanogr 63(6):2307–2320

    Article  Google Scholar 

  • Benaltabet T, Lapid G, Torfstein A (2022) Dissolved aluminium dynamics in response to dust storms, wet deposition, and sediment resuspension in the Gulf of Aqaba, northern Red Sea. Geochim Cosmochim Acta 335:137–154

    Article  Google Scholar 

  • Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ (2013) Trichodesmium—a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev 37(3):286–302

    Article  Google Scholar 

  • Bronk DA, Steinberg DK (2008) Chapter 8—Nitrogen regeneration. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, San Diego, pp 385–467

    Chapter  Google Scholar 

  • Buesseler KO, Boyd PW, Black EE, Siegel DA (2020) Metrics that matter for assessing the ocean biological carbon pump. Proc Natl Acad Sci 117(18):9679–9687

    Article  Google Scholar 

  • Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ (1997) Trichodesmium, a globally significant marine cyanobacterium. Science 276:1221–1229

    Article  Google Scholar 

  • Carpenter EJ, Capone DG (2008) Chapter 4—Nitrogen fixation in the marine environment. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, San Diego, pp 141–198

    Chapter  Google Scholar 

  • Coles VJ, Hood RR, Pascual M, Capone DG (2004) Modeling the impact of Trichodesmium and nitrogen fixation in the Atlantic Ocean. J Geophys Res Oceans 109(C6):C06007

    Article  Google Scholar 

  • Dixit S, Van Cappellen P, van Bennekom AJ (2001) Processes controlling solubility of biogenic silica and pore water build-up of silicic acid in marine sediments. Mar Chem 73(3–4):333–352

    Article  Google Scholar 

  • Field AP (2009) Discovering statistics using SPSS (and sex and drugs and rock ‘n’ roll). SAGE, Singapore

    Google Scholar 

  • Gledhill M, Basu S, Shaked Y (2019) Metallophores associated with Trichodesmium erythraeum colonies from the Gulf of Aqaba. Metallomics 11(9):1547–1557

    Article  Google Scholar 

  • Hemingway JD, Rothman DH, Grant KE, Rosengard SZ, Eglinton TI, Derry LA, Galy VV (2019) Mineral protection regulates long-term global preservation of natural organic carbon. Nature 570(7760):228–231

    Article  Google Scholar 

  • Hong H, Shen R, Zhang F, Wen Z, Chang S, Lin W, Kranz SA, Luo Y-W, Kao S-J, Morel FMM, Shi D (2017) The complex effects of ocean acidification on the prominent N2-fixing cyanobacterium Trichodesmium. Science 356(6337):527–531

    Article  Google Scholar 

  • Kienast SS, Winckler G, Lippold J, Albani S, Mahowald NM (2016) Tracing dust input to the global ocean using thorium isotopes in marine sediments: ThoroMap. Global Biogeochem Cycles 30(10):1526–1541

    Article  Google Scholar 

  • Lambert F, Delmonte B, Petit JR, Bigler M, Kaufmann PR, Hutterli MA, Stocker TF, Ruth U, Steffensen JP, Maggi V (2008) Dust-climate couplings over the past 800,000 years from the EPICA Dome C ice core. Nature 452(7187):616–619

    Article  Google Scholar 

  • Liu J, Zhou L, Li G, Ke Z, Shi R, Tan Y (2018) Beneficial effects of aluminum enrichment on nitrogen-fixing cyanobacteria in the South China Sea. Mar Pollut Bull 129(1):142–150

    Article  Google Scholar 

  • Liu J, Zhou L, Ke Z, Li G, Tan Y (2020) Phosphorus deficiency induced by aluminum in a marine nitrogen-fixing cyanobacterium Crocosphaera watsonii WH0003. Chemosphere 246:125641

    Article  Google Scholar 

  • Martin JH (1990) Glacial-interglacial CO2 change: the Iron Hypothesis. Paleoceanography 5(1):1–13

    Article  Google Scholar 

  • Martin JH, Knauer GA, Karl DM, Broenkow WW (1987) VERTEX: carbon cycling in the northeast Pacific. Deep Sea Res Part A Oceanogr Res Pap 34(2):267–285

    Article  Google Scholar 

  • Menzel Barraqueta J-L, Samanta S, Achterberg EP, Bowie AR, Croot P, Cloete R, De Jongh T, Gelado-Caballero MD, Klar JK, Middag R, Loock JC, Remenyi TA, Wenzel B, Roychoudhury AN (2020) A first global oceanic compilation of observational dissolved aluminum data with regional statistical data treatment. Front Mar Sci 7:468

    Article  Google Scholar 

  • Merino C, Fontaine S, Palma G, Matus F (2017) Effect of aluminium on mineralization of water extractable organic matter and microbial respiration in southern temperate rainforest soils. Eur J Soil Biol 82:56–65

    Article  Google Scholar 

  • Miklasz KA, Denny MW (2010) Diatom sinking speeds: improved predictions and insight from a modified Stokes’ law. Limnol Oceanogr 55(6):2513–2525

    Article  Google Scholar 

  • Moore CM, Mills MM, Achterberg EP, Geider RJ, LaRoche J, Lucas MI, McDonagh EL, Pan X, Poulton AJ, Rijkenberg MJ (2009) Large-scale distribution of Atlantic nitrogen fixation controlled by iron availability. Nat Geosci 2(12):867–871

    Article  Google Scholar 

  • Moran SB, Moore RM (1991) The potential source of dissolved aluminum from resuspended sediments to the North Atlantic Deep Water. Geochim Cosmochim Acta 55(10):2745–2751

    Article  Google Scholar 

  • Rijkenberg MJA, Langlois RJ, Mills MM, Patey MD, Hill PG, Nielsdóttir MC, Compton TJ, LaRoche J, Achterberg EP (2011) Environmental forcing of nitrogen fixation in the eastern tropical and sub-tropical North Atlantic Ocean. PLoS ONE 6(12):e28989

    Article  Google Scholar 

  • Stoffyn-Egli P (1982) Dissolved aluminium in interstitial waters of recent terrigenous marine sediments from the North Atlantic Ocean. Geochim Cosmochim Acta 46(8):1345–1352

    Article  Google Scholar 

  • Tovar-Sanchez A, Sanudo-Wilhelmy SA, Kustka AB, Agusti S, Dachs J, Hutchins DA, Capone DG, Duarte CM (2006) Effects of dust deposition and river discharges on trace metal composition of Trichodesmium spp. in the tropical and subtropical North Atlantic Ocean. Limnol Oceanogr 51(4):1755–1761

    Article  Google Scholar 

  • Van Cappellen P, Dixit S, van Beusekom J (2002) Biogenic silica dissolution in the oceans: reconciling experimental and field-based dissolution rates. Global Biogeochem Cycles 16(4):1075

    Google Scholar 

  • van Hulten MMP, Sterl A, Tagliabue A, Dutay JC, Gehlen M, de Baar HJW, Middag R (2013) Aluminium in an ocean general circulation model compared with the West Atlantic Geotraces cruises. J Mar Syst 126:3–23

    Article  Google Scholar 

  • Wagai R, Kajiura M, Asano M (2020) Iron and aluminum association with microbially processed organic matter via meso-density aggregate formation across soils: organo-metallic glue hypothesis. SOIL 6(2):597–627

    Article  Google Scholar 

  • White AE, Spitz YH, Karl DM, Letelier RM (2006) Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications. Limnol Oceanogr 51(4):1777–1790

    Article  Google Scholar 

  • Zehr JP, Capone DG (2020) Changing perspectives in marine nitrogen fixation. Science 368(6492):aay9514

    Article  Google Scholar 

  • Zhang F, Hong H, Kranz SA, Shen R, Lin W, Shi D (2019) Proteomic responses to ocean acidification of the marine diazotroph Trichodesmium under iron-replete and iron-limited conditions. Photosynth Res 142(1):17–34

    Article  Google Scholar 

  • Zhang F, Wen Z, Wang S, Tang W, Luo Y-W, Kranz SA, Hong H, Shi D (2022) Phosphate limitation intensifies negative effects of ocean acidification on globally important nitrogen fixing cyanobacterium. Nat Commun 13(1):6730

    Article  Google Scholar 

  • Zhou L, Tan Y, Huang L, Wang W-X (2016) Enhanced utilization of organic phosphorus in a marine diatom Thalassiosira weissflogii: a possible mechanism for aluminum effect under P limitation. J Exp Mar Biol Ecol 478:77–85

    Article  Google Scholar 

  • Zhou L, Liu J, Xing S, Tan Y, Huang L (2018a) Phytoplankton responses to aluminum enrichment in the South China Sea. J Inorg Biochem 181:117–131

    Article  Google Scholar 

  • Zhou L, Tan Y, Huang L, Fortin C, Campbell PGC (2018b) Aluminum effects on marine phytoplankton: implications for a revised Iron Hypothesis (Iron-Aluminum Hypothesis). Biogeochemistry 139(2):123–137

    Article  Google Scholar 

  • Zhou L, Liu F, Liu Q, Fortin C, Tan Y, Huang L, Campbell PGC (2021) Aluminum increases net carbon fixation by marine diatoms and decreases their decomposition: evidence for the iron–aluminum hypothesis. Limnol Oceanogr 66(7):2712–2727

    Article  Google Scholar 

  • Zhou L, Huang L, Tan Y (2023) Iron-aluminum hypothesis and the potential of ocean aluminum fertilization as a carbon dioxide removal strategy. J Trop Oceanogr 42(3):1–18 (in Chinese with English abstract)

    Google Scholar 

Download references

Acknowledgements

We thank Kim Racine and Lise Rancourt at the Institut national de la Recherche scientifique for their technical assistance. We also thank the data archive support from the National Earth System Data Center, National Science & Technology Infrastructure of China (http://www.geodata.cn).

Funding

This work was supported by the National Natural Science Foundation of China (41506150), the Natural Sciences and Engineering Research Council of Canada (NSERC), the Guangdong Basic and Applied Basic Research Foundation (2019A1515011645), the Development Fund of South China Sea Institute of Oceanology of the Chinese Academy of Sciences (SCSIO202204), the Science and Technology Planning Project of Guangdong Province, China (2020B1212060058). C. Fortin and P. G. C. Campbell were supported by the Canada Research Chairs Program. L. Zhou was supported by a Chinese Academy of Sciences Scholarship. F. Liu is supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie Grant Agreement No. 891418 and UK Natural Environment Research Council Grant NE/V01451X/1.

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by LZ and FL. The first draft of the manuscript was written by LZ and all authors commented on subsequent versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Linbin Zhou or Yehui Tan.

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Zhou, L., Liu, F., Tan, Y. et al. Aluminum-induced changes in the net carbon fixation and carbon decomposition of a nitrogen-fixing cyanobacterium Trichodesmium erythraeum. Biogeochemistry 165, 277–290 (2023). https://doi.org/10.1007/s10533-023-01081-4

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