The environmental, elemental and proteomic plasticity of Trichodesmium in the (sub) tropical atlantic

Abstract

Phytoplankton dominate surface ocean biomass and have major roles in global carbon and nutrient cycling. Of these, the cyanobacterial Trichodesmium sp. are considered the dominant and most conspicuous nitrogen fixers in the tropical and subtropical oceans, regimes frequently characterised by low concentrations of fixed nitrogen.
Despite being arguably the best studied marine diazotroph, the factors controlling the distribution and growth of Trichodesmium remain a subject of debate, with sea surface temperature, the partial pressure of CO2 and nutrients including iron and phosphorus, all suggested to be important. Dominant controls on the biogeography of other important marine diazotrophic organisms are even less clear. Synthesising data from 7 research cruises collectively spanning large temporal and spatial scales across the Atlantic Ocean, including 2 previously unreported studies crossing the largely under-sampled South Atlantic gyre, we assessed the relationship between proposed environmental drivers and both community nitrogen fixation rates and the distribution of Trichodesmium. Simple linear regression analysis of the combined data set would suggest no relationship between any of the sampled environmental variables and nitrogen fixation rates. However, considering the concentrations of iron and phosphorus together within a resource-ratio framework indicates the combined effects these nutrients have on Trichodesmium and broader diazotroph biogeography. The resource ratio framework is argued to be consistent with both the previously described North-South Atlantic contrast in Trichodesmium abundance, and the presence and consequence of a substantial non-Trichodesmium diazotrophic community in the euphotic zone of the western South Atlantic subtropical gyre.
Using high-throughput chemical and biological analyses we were able to observe significant plasticity in Trichodesmium’s elemental composition. The macro- and micro- elemental composition of environmental Trichodesmium showed enrichments in arsenic, vanadium and molybdenum along an environmental phosphorus gradient, which we attributed to phosphorus- stress induced accidental uptake. Stoichiometric comparison with bulk phytoplankton revealed enrichments in iron (alongside nickel, copper and zinc) to which we predict 12-37% is attributed to the process of nitrogen fixation.
To date, understanding Trichodesmium’s propensity for growth in iron-deplete oceanic regimes has focused on traditional metrics such as physiological rates and targeted molecular studies. Here a labelfree quantitative proteomics technique (MSE) was employed to examine the full complement of Trichodesmium erythraeum IMS101’s proteome when grown with different iron availability. Iron stress resulted in increased abundances in proteins involved in iron-stress acclimation and of proteins involved in iron-uptake. Also a systematic decrease in the iron-binding proteins involved in photosynthesis and nitrogen fixation is reported. Such changes reveal potentially novel iron uptake pathways but also that Trichodesmium reallocates resource away from nitrogen fixation and towards components of the photosynthetic apparatus under iron stress.
Finally, utilising a bioinformatic approach we are able to generate a predicted metallo-proteome for Trichodesmium, detailing the relative protein-bound concentrations of iron, vanadium, arsenic, molybdenum, zinc, nickel, copper, manganese, cadmium and cobalt. By comparing this metallo-proteome to the observed intracellular metallome we were able to synthesise our findings into the description of discreet Trichodesmium phenotypes observed in the (sub)-tropical Atlantic. In doing so, we present a comprehensive, observation-based explanation of the interactions between Trichodesmium and iron, linking small scale physiology to basin-scale biogeochemical variability.

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ORCID for C.M. Moore: orcid.org/0000-0002-9541-6046

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