Cyanobacterial Cultures, Cell Extracts, and Individual Toxins Decrease Photosynthesis in the Terrestrial Plants Lactuca sativa and Zea mays

Abstract

Cyanobacterial harmful algal blooms (cHABs) are increasing due to eutrophication and climate change, as is irrigation of crops with freshwater contaminated with cHAB toxins. A few studies, mostly in aquatic protists and plants, have investigated the effects of cHAB toxins or cell extracts on various aspects of photosynthesis, with variable effects reported (negative to neutral to positive). We examined the effects of cyanobacterial live cultures and cell extracts (Microcystis aeruginosa or Anabaena flos-aquae) and individual cHAB toxins (anatoxin-a, ANA; beta-methyl-amino-L-alanine, BMAA; lipopolysaccharide, LPS; microcystin-LR, MC-LR) on photosynthesis in intact plants and leaf pieces in corn (Zea mays) and lettuce (Lactuca sativa). In intact plants grown in soil or hydroponically, overall net photosynthesis (Pn), but not Photosystem-II (PSII) electron-transport yield (ΦPSII), decreased when roots were exposed to cyanobacterial culture (whether with intact cells, cells removed, or cells lysed and removed) or individual toxins in solution (especially ANA, which also decreased rubisco activity); cyanobacterial culture also decreased leaf chlorophyll concentration. In contrast, ΦPSII decreased in leaf tissue vacuum-infiltrated with cyanobacterial culture or the individual toxins, LPS and MC-LR, though only in illuminated (vs. dark-adapted) leaves, and none of the toxins caused significant decreases in in vitro photosynthesis in thylakoids. Principal component analysis indicated unique overall effects of cyanobacterial culture and each toxin on photosynthesis. Hence, while cHAB toxins consistently impacted plant photosynthesis at ecologically relevant concentrations, the effects varied depending on the toxins and the mode of exposure.