Grazer-induced changes in molecular signatures of cyanobacteria

• Published in: Algal research (Amsterdam) 2022-01, Vol.61, p.102575, Article 102575
• Main Authors: Nguyen, Don D., Sauer, Jonathan S., Camarda, Luis P., Sherman, Summer L., Prather, Kimberly A., Golden, Susan S., Pomeroy, Robert, Dorrestein, Pieter C., Simkovsky, Ryan
• Format: Article
• Language: English
• Subjects: Chlorophyll; Cyanobacteria; Grazers; Imaging mass spectrometry; Molecular ecology; VOCs
• ISSN: 2211-9264; 2211-9264
• DOI: 10.1016/j.algal.2021.102575

Algal biomass production is an emerging renewable source of fuels, nutrients, manufacturing materials, and pharmaceuticals. Industrial-scale production is predominantly performed in open raceway ponds that are inexpensive to build, operate, and maintain compared to closed bioreactors. However, these open pond systems suffer from increased opportunities for biological contamination from predators, pathogens, and competitors, which result in reduced biomass quality and yields and often the complete destruction of the crop over a short period of time. Early detection of contaminants is a necessary step of integrated pest management for triggering and informing interventions to prevent crop losses. To develop a sensitive method of detection utilizing mass spectrometry (MS), we used three methods – imaging mass spectrometry (imaging MS), liquid chromatography MS/MS (LC-MS/MS) combined with molecular networking, and gas chromatography MS/MS (GC–MS/MS) – to observe and identify molecular signatures from a model predator-prey system of the heterolobosean amoeba HGG1 preying on the filamentous cyanobacterium Anabaena sp. PCC 7120. Imaging MS enabled the association of molecules with the crop, the predator, or the activity of protozoan grazing, while LC-MS/MS-based molecular networking identified a subset of the grazing-specific signals as the chlorophyll breakdown products pyropheophytin, pheophorbide A, and pyropheophorbide. Application of MS techniques to other amoeba-cyanobacterial predator-prey pairs allowed categorization of grazing signatures as universal or specific to the species of prey, predator, or the prey-predator pairing, indicating that MS-based techniques can distinguish crops from competitors and potentially identify predators. Finally, GCMS/MS was shown to be capable of monitoring novel volatile organic compounds (VOCs), including those predicted to be released through chlorophyll breakdown, in the headspace over algal cultures under predation. These results demonstrate that the combination of multiple MS technologies creates a predictive framework to identify and catalog relevant molecular signatures for informing crop protection strategies. [Display omitted] •Solid, liquid, and gas phase mass spectrometry of amoebal grazing on cyanobacteria•Chlorophyll breakdown products and pathways can be used as grazing signatures.•Diverse predator-prey pairs categorize signatures as both universal and species-specific.•MALDI imaging MS and HPLC-MS predict vo