How Copepods Can Eat Toxins Without Getting Sick: Gut Bacteria Help Zooplankton to Feed in Cyanobacteria Blooms

Abstract

Toxin-producing cyanobacteria can be harmful to aquatic biota, although some grazers utilize them with often beneficial effects on their growth and reproduction. It is commonly assumed that gut microbiota facilitates host adaptation to the diet; however, the evidence for adaptation mechanisms is scarce. Here, we investigated the abundance of mlrA genes in the gut of the Baltic copepods Acartia bifilosa and Eurytemora affinis during cyanobacteria bloom season (August) and outside it (February). The mlrA genes are unique to microcystin and nodularin degraders, thus indicating the capacity to break down these toxins by the microbiota. The mlrA genes were expressed in the copepod gut year-round, being >10-fold higher in the summer than in the winter populations. Moreover, they were significantly more abundant in Eurytemora than Acartia. To understand the ecological implications of this variability, we conducted feeding experiments using summer- and winter-collected copepods to examine if/how the mlrA abundance in the microbiota affect: (1) uptake of toxic Nodularia spumigena, (2) uptake of a non-toxic algal food offered in mixtures with N. spumigena, and (3) concomitant growth potential in the copepods. The findings provide empirical evidence that the occurrence of mlrA genes in the copepod microbiome facilitates nutrient uptake and growth when feeding on phytoplankton mixtures containing nodularin-producing cyanobacteria; thus, providing an adaptation mechanism to the cyanobacteria blooms.

Antioxidant Responses in Copepods Are Driven Primarily by Food Intake, Not by Toxin-Producing Cyanobacteria in the Diet

“…In E. affinis co-occurring with cyanobacterial blooms, positive effects of Nodularia ingestion on growth, reproductive output, and naupliar survival have been reported ( Hogfors et al, 2014 ; Motwani et al, 2017 ), indicating that all ontogenetic stages of this species are well-adapted to the cyanotoxins and can efficiently utilize toxin-producing cyanobacteria. Recently, the mechanism for the species-specific growth responses to hepatotoxin-producing cyanobacteria was proposed ( Gorokhova et al, 2021 ). This mechanism is based on environmental and genetic adaptation in the copepod microbiome that harbors higher abundances of toxin-degrading bacteria in E. affinis than in A. bifilosa .…”

“…In line with this, low toxin retention (Guisande et al, 2002;Karjalainen et al, 2003;Kozlowsky-Suzuki et al, 2009) suggests that fairly efficient detoxification mechanisms may exist in these and, probably, other animals co-existing with toxic blooms, making them relevant as test species for ecotoxicological surveys. However, we expected to find stronger diet effects in A. bifilosa than E. affinis because of the higher sensitivity of the former to the cyanobacteria diet manifested as adverse effects on growth and reproduction reported in the field and laboratory studies (Motwani et al, 2017;Gorokhova et al, 2021).…”

“…Most laboratory studies of mesozooplankton grazing on natural plankton assemblages show avoidance of cyanobacteria and preferential feeding on non-toxic strains ( Lampert, 1987 ; Sellner et al, 1996 ). However, the evidence is accumulating that cyanobacteria contribute substantially to the diets of some copepods and mysids in situ ( Kozlowsky-Suzuki et al, 2003 ; Peters et al, 2006 ; Gorokhova, 2009 ; Motwani et al, 2017 ; Gorokhova et al, 2021 ). Coevolutionary histories, regular exposure, and high ingestion of toxic cyanobacteria support the idea that these animals might cope with ingested toxins.…”

“…Coevolutionary histories, regular exposure, and high ingestion of toxic cyanobacteria support the idea that these animals might cope with ingested toxins. Moreover, toxin biodegradation of the copepod gut microbiome has been recently proposed as a mechanism behind successful feeding and growth during cyanobacterial blooms ( Gorokhova et al, 2021 ). However, this does not mean that chronic exposure to the high abundances of the toxin-producing cyanobacteria induces no adverse sublethal effects.…”

High capacity for a dietary specialist consumer population to cope with increasing cyanobacterial blooms

“…However, in freshwater lakes 29 and the Baltic Sea 30,31 , various grazers have evolved physiological and behavioral adaptations, enhancing their ability to coexist with toxic cyanobacteria. Moreover, significant variability in growth and other fitness-related traits between Baltic copepod species feeding on Nodularia-rich diets has been observed and attributed to various adaptation mechanisms, including nodularin biodegraders in the host microbiome 32 .…”