Abstract
Non-proteinogenic neurotoxic amino acid β-N-methylamino-L-alanine (BMAA) is synthesized by cyanobacteria, diatoms, and dinoflagellates, and is known to be a causative agent of human neurodegenerative diseases. Different phytoplankton organisms’ ability to synthesize BMAA could indicate the importance of this molecule in the interactions between microalgae in nature. We were interested in the following: what kinds of mechanisms underline BMAA’s action on cyanobacterial cells in different nitrogen supply conditions. Herein, we present a proteomic analysis of filamentous cyanobacteria Nostoc sp. PCC 7120 cells that underwent BMAA treatment in diazotrophic conditions. In diazotrophic growth conditions, to survive, cyanobacteria can use only biological nitrogen fixation to obtain nitrogen for life. Note that nitrogen fixation is an energy-consuming process. In total, 1567 different proteins of Nostoc sp. PCC 7120 were identified by using LC-MS/MS spectrometry. Among them, 123 proteins belonging to different functional categories were selected—due to their notable expression differences—for further functional analysis and discussion. The presented proteomic data evidences that BMAA treatment leads to very strong (up to 80%) downregulation of α (NifD) and β (NifK) subunits of molybdenum-iron protein, which is known to be a part of nitrogenase. This enzyme is responsible for catalyzing nitrogen fixation. The genes nifD and nifK are under transcriptional control of a global nitrogen regulator NtcA. In this study, we have found that BMAA impacts in a total of 22 proteins that are under the control of NtcA. Moreover, BMAA downregulates 18 proteins that belong to photosystems I or II and light-harvesting complexes; BMAA treatment under diazotrophic conditions also downregulates five subunits of ATP synthase and enzyme NAD(P)H-quinone oxidoreductase. Therefore, we can conclude that the disbalance in energy and metabolite amounts leads to severe intracellular stress that induces the upregulation of stress-activated proteins, such as starvation-inducible DNA-binding protein, four SOS-response enzymes, and DNA repair enzymes, nine stress-response enzymes, and four proteases. The presented data provide new leads into the ecological impact of BMAA on microalgal communities that can be used in future investigations.
Highlights
Prokaryotic and eukaryotic phytoplankton species, such as cyanobacteria, diatoms, and dinoflagellates, synthesize many different secondary metabolites of ecological and practical significance [1,2]
To elucidate the effect of BMAA on Nostoc PCC 7120 under diazotrophic conditions cyanobacteria cells were grown in three independent biological replicates in nitrogen-free
BG110 medium for 48 h in two experimental settings, in which: (1) control samples consisted of cells grown without BMAA addition and (2) treated samples contained cells grown with BMAA (20 μmol), as it was performed before [23,24]
Summary
Prokaryotic and eukaryotic phytoplankton species, such as cyanobacteria (cyanoprokaryota), diatoms, and dinoflagellates, synthesize many different secondary metabolites of ecological and practical significance [1,2]. Among them stands out the non-proteinogenic neurotoxic amino acid β-N-methylamino-L-alanine (BMAA), which was related to human neurodegenerative diseases [3,4,5]. The ability of many different microalgae species to synthesize BMAA in a wide range of concentrations—from nanograms to thousands of micrograms per gram of dry weight [6,7,8]—may indicate the biological meaning of this molecule in their life [9,10,11,12]. It was discovered that non-diazotrophic unicellular cyanobacteria start to produce BMAA in nitrogen-limited conditions [13]. Cyanobacteria are able to produce BMAA but can adsorb this amino acid.
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