Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

Basu, Subhajit; Gledhill, Martha; Beer, Dirk de; Matondkar, S.G.P.; Shaked, Yeala

doi:10.1038/s42003-019-0534-z

Cited by 66 publications

(87 citation statements)

References 40 publications

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“…3F, p = 0.04), and a TonB dependent transporter (TBDT) for ferrienterochelin/colicins was identified only in puffs with particles 24 . This corroborates earlier evidence that though Trichodesmium does not produce its own siderophores, it acquires siderophore-bound iron produced via mutualistic interactions with epibionts, especially when provided with concentrated dust 8,25 .…”

Section: Resultssupporting

confidence: 91%

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Held

Sutherland

Webb

et al. 2020

Preprint

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The keystone marine nitrogen fixer Trichodesmium thrives in high dust environments, and while experimental observations suggest that Trichodesmium colonies can access the essential nutrient iron from dust particles, it is not known the extent to which this occurs in the field. Here we demonstrate that Trichodesmium colonies actively process mineral particles in nature with direct molecular impacts. Microscopy and synchrotron-based imaging demonstrated heterogeneous associations with particles consistent with iron oxide and iron silicate minerals. Metaproteomic analysis of individual colonies revealed enrichment of biogeochemically-relevant proteins including photosynthesis proteins and metalloproteins containing iron, nickel, copper and zinc when particles were present. The iron-storage protein ferritin was particularly enriched implying accumulation of particle-derived iron, and multiple iron acquisition pathways including Fe(II), Fe(III), and Fe-siderophore transporters were engaged, including evidence of superoxide-driven particle dissolution. While the particles clearly provided iron, there was also evidence that the concentrated metals had toxic effects. The molecular mechanisms allowing Trichodesmium to interact with particulate minerals are fundamental to its success and global impact on nitrogen biogeochemistry, and may contribute to the leaching of particulate trace metals with implications for global iron and carbon cycling.

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Section: Resultssupporting

confidence: 91%

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Held

Sutherland

Webb

et al. 2020

Preprint

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“…For example, about half of the genomes that produce siderophores can produces vibrioferrin (~15% of total genomes), yet the vibrioferrin-bound iron is likely accessible to many more organisms, including phytoplankton, upon photolysis (18). Thus, in agreement with recent considerations (75), we highlight the role of siderophores as "keystone molecules" (76) and take this as an indication that the organisms producing them have an important role in the functionality of microbial communities (e.g., references (77,78)).…”

Section: Production Of Phytohormones and Siderophores -Common Mechanisupporting

confidence: 84%

Comparative whole-genome approach to identify bacterial traits for microbial interactions

Zoccarato

Sher

Miki

et al. 2020

Preprint

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ABSTRACTInteractions among microorganisms affect the structure and function of microbial communities, with potentially far-reaching effects on ecosystem health and biogeochemical cycles. The functional traits mediating microbial interactions are known for several model organisms, but the prevalence of these traits across microbial diversity is unknown. We developed a new genomic approach to systematically explore the occurrence of metabolic functions and specific interaction traits (e.g. the production of vitamins, siderophores, antimicrobial compounds and phytohormones), and apply this approach to 473 sequenced genomes from marine bacteria. We identify 48 coherent genome functional clusters (GFCs), that are partly consistent with known bacterial ecotypes (e.g. within pico-Cyanobacteria and Vibrio taxa) and identify putative new ones (e.g. Marinobacter, Alteromonas and Pseudoalteromonas). Interaction traits such as the production of and resistance towards antimicrobial compounds and the production of phytohormones are widely distributed among the GFCs, while other traits are less common (e.g. siderophores and secretion systems are found in 32% of genomes or less). Several GFCs lack the ability to produce B vitamins, suggesting that these metabolites represent essential trading goods for many bacteria. Alpha- and Gammaproteobacteria encode many interaction traits, and appear particularly poised to interact both synergistically and antagonistically with co-occurring bacteria and phytoplankton. Linked Trait Clusters (LTCs) group chemotaxis, motility and adhesion with regulatory systems involved in virulence and biofilm formation, and suggest that type-4 secretion systems may be used to inject the hormone indole acetic acid into target phytoplankton cells. Similar efficient processing and representation of multidimensional microbial functional information will be increasingly essential for translating genomes into ecosystem understanding across biomes.

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“…Next, we tested to what extent respiration by bacteria associated with Trichodesmium can lower O 2 concentrations in the colonies. In a first approach, we added two different bacterial strains originally isolated from Trichodesmium in Eilat (Basu et al ) to freshly collected colonies. While the initial abundance of (naturally occurring) bacteria in these colonies could not be quantified, we assumed a similar abundance as during a comparable sampling campaign at the same location (7.5 ± 0.46 × 10 4 cells colony −1 ; Basu and Shaked ).…”

Section: Resultsmentioning

confidence: 99%

“…Since ferrihydrite is not internalized directly by Trichodesmium (Rubin et al ), the surplus uptake over abiotic dissolution implies that Trichodesmium biologically enhanced ferrihydrite dissolution, in a process that may involve reductive and/or ligand‐promoted dissolution, in agreement with previous reports by Basu and Shaked (). Production of iron‐binding ligands (siderophores) by the Trichodesmium consortium was recently documented in the Gulf of Eilat (Gledhill et al ) and shown to increase ferrihydrite bioavailability by promoting its dissolution (Basu et al ). To specifically test for microenvironment effects on ligand‐promoted dissolution, four of the uptake experiments were conducted in the presence of the iron‐binding ligand DFB (March 27 th till March 29 th ; Fig.…”

Section: Resultsmentioning

confidence: 99%

Mineral iron dissolution in Trichodesmium colonies: The role of O₂ and pH microenvironments

Eichner

Basu

Wang

et al. 2019

Limnology & Oceanography

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Colonies of the N2‐fixing cyanobacterium Trichodesmium can harbor distinct chemical microenvironments that may assist the colonies in acquiring mineral iron from dust. Here, we characterized O2 and pH gradients in and around Trichodesmium colonies by microsensor measurements on > 170 colonies collected in the Gulf of Eilat over ∼ 2 months. O2 concentrations and pH values in the center of single colonies decreased in the dark due to respiration, reaching minimum values of 70 μmol L−1 and 7.7, whereas in the light, O2 and pH increased due to photosynthesis, reaching maximum values of 410 μmol L−1 and 8.6. Addition of dust and bacteria and increasing colony size influenced O2 and pH levels in the colonies, yet values remained within the range observed in single natural colonies. However, lower values down to 60 μmol L−1 O2 and pH 7.5 were recorded in the dark in dense surface accumulations of Trichodesmium. Using radiolabelled ferrihydrite, we examined the effect of these conditions on mineral iron dissolution and availability to Trichodesmium. Dark‐incubated colonies did not acquire iron from ferrihydrite faster than light‐incubated colonies, indicating that the dark‐induced decrease in pH and O2 within single colonies is too small to significantly increase mineral iron bioavailability. Yet, ligand‐promoted dissolution of ferrihydrite, a mechanism likely applied by Trichodesmum for acquiring mineral iron, did increase at the lower pH levels observed in surface accumulations. Thus, Trichodesmium surface blooms in their final stage may harbor chemical conditions that enhance the dissolution and bioavailability of mineral iron to the associated microbial community.

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Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

Cited by 66 publications

References 40 publications

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Comparative whole-genome approach to identify bacterial traits for microbial interactions

Mineral iron dissolution in Trichodesmium colonies: The role of O₂ and pH microenvironments

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Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust

Cited by 66 publications

References 40 publications

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Mechanisms and heterogeneity of mineral use by natural colonies of the cyanobacteriumTrichodesmium

Comparative whole-genome approach to identify bacterial traits for microbial interactions

Mineral iron dissolution in Trichodesmium colonies: The role of O2 and pH microenvironments

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Mineral iron dissolution in Trichodesmium colonies: The role of O₂ and pH microenvironments