Copepods drive large-scale trait-mediated effects in marine plankton

Selander, Erik; Berglund, E. Carina; Engström, Pia; Berggren, Fredrik; Eklund, Johan; Harðardóttir, Sara; Lundholm, Nina; Grebner, Wiebke; Andersson, Mats X.

doi:10.1126/sciadv.aat5096

Cited by 80 publications

(96 citation statements)

References 32 publications

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“…Presently, 21 copepodamide compounds have been identified and their composition is copepod species specific [10]. Pseudo-nitzschia seriata increases DA production as a response to the naturally occurring mixture of copepods and to at least three isolated copepodamides in ecosystem-relevant doses [10,11]. Cellular signal transduction depends on the perception of external cues, but how the diatoms or other phytoplankton species perceive the predator cues is still poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

et al. 2019

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Background A major cause of phytoplankton mortality is predation by zooplankton. Strategies to avoid grazers have probably played a major role in the evolution of phytoplankton and impacted bloom dynamics and trophic energy transport. Certain species of the genus Pseudo-nitzschia produce the neurotoxin, domoic acid (DA), as a response to the presence of copepod grazers, suggesting that DA is a defense compound. The biosynthesis of DA comprises fusion of two precursors, a C10 isoprenoid geranyl pyrophosphate and l -glutamate. Geranyl pyrophosphate (GPP) may derive from the mevalonate isoprenoid (MEV) pathway in the cytosol or from the methyl-erythritol phosphate (MEP) pathway in the plastid. l -glutamate is suggested to derive from the citric acid cycle. Fragilariopsis , a phylogenetically related but nontoxic genus of diatoms, does not appear to possess a similar defense mechanism. We acquired information on genes involved in biosynthesis, precursor pathways and regulatory functions for DA production in the toxigenic Pseudo-nitzschia seriata , as well as genes involved in responses to grazers to resolve common responses for defense strategies in diatoms. Results Several genes are expressed in cells of Pseudo-nitzschia when these are exposed to predator cues. No genes are expressed in Fragilariopsis when treated similarly, indicating that the two taxa have evolved different strategies to avoid predation. Genes involved in signal transduction indicate that Pseudo-nitzschia cells receive signals from copepods that transduce cascading molecular precursors leading to the formation of DA. Five out of seven genes in the MEP pathway for synthesis of GPP are upregulated, but none in the conventional MEV pathway. Five genes with known or suggested functions in later steps of DA formation are upregulated. We conclude that no gene regulation supports that l -glutamate derives from the citric acid cycle, and we suggest the proline metabolism to be a downstream precursor. Conclusions Pseudo-nitzschia cells, but not Fragilariopsis , receive and respond to copepod cues. The cellular route for the C10 isoprenoid product for biosynthesis of DA arises from the MEP metabolic pathway and we suggest proline metabolism to be a downstream precursor for l -glutamate. We suggest 13 genes with unknown function to be involved in diatom responses to grazers. Electronic supplementary material The online version of this article (10.1186/s12867-019-0124-0) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

et al. 2019

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“…The time scale to reach this equilibrium is k −1 . For typical values ( Table 1) the equilibrium concentration is~30 pM which is reached in a time scale of~5 h. This is an order of magnitude higher than the highest concentrations found in situ [9] which suggest that copepods do not reside sufficiently long in the same water package, or that other loss factors such as vertical mixing and sedimentation removes copepodamides. Alternatively, the production rate of copepodamides reported for Calanus sp.…”

Section: Background Concentrationmentioning

confidence: 84%

“…Even for strong turbulence, the constant supply of copepodamides from copepods will cause an increase in background concentration, which when sufficiently large will be balanced by the decay rate of the solute. These background concentrations reach bioactive concentrations in the upper ocean that trigger defensive traits such as harmful algal toxin production [9]. Since zooplankton migrate to deeper waters during daytime to avoid visual predators, the concentration will oscillate.…”

Section: Background Concentrationmentioning

confidence: 99%

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Chemical Signaling in the Turbulent Ocean—Hide and Seek at the Kolmogorov Scale

Selander

Fredriksson

Arneborg

2020

Fluids

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Chemical cues and signals mediate resource acquisition, mate finding, and the assessment of predation risk in marine plankton. Here, we use the chemical properties of the first identified chemical cues from zooplankton together with in situ measurements of turbulent dissipation rates to calculate the effect of turbulence on the distribution of cues behind swimmers as well as steady state background concentrations in surrounding water. We further show that common zooplankton (copepods) appears to optimize mate finding by aggregating at the surface in calm conditions when turbulence do not prevent trail following. This near surface environment is characterized by anisotropic turbulence and we show, using direct numerical simulations, that chemical cues distribute more in the horizontal plane than vertically in these conditions. Zooplankton may consequently benefit from adopting specific search strategies near the surface as well as in strong stratification where similar flow fields develop. Steady state concentrations, where exudation is balanced by degradation develops in a time scale of~5 h. We conclude that the trails behind millimeter-sized copepods can be detected in naturally occurring turbulence below the wind mixed surface layer or in the absence of strong wind. The trails, however, shorten dramatically at high turbulent dissipation rates, above~10 −3 cm 2 s −3 (10 −7 W kg −1 ) Fluids 2020, 5, 54 2 of 11 animals in the sea, copepods, are all in this size range, 100 µm to a few mm, and may even traverse the Kolmogorov scale when growing up from larval stages to adults (Figure 1).

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“…negatively at intra-and interspecific levels (eg John et al 2015). Notably, these compounds may function as intentional "signals" (eg a sexual attractant released by a sender) or as unintentionally released "cues" (eg prey-specific chemicals that attract predators [Steiger et al 2011] or warn prey of predator presence [Selander et al 2015[Selander et al , 2019).…”

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confidence: 99%

Using chemical language to shape future marine health

Saha

Berdalet

Carotenuto

et al. 2019

Frontiers in Ecol & Environ

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“Infochemicals” (information‐conveying chemicals) dominate much of the underwater communication in biological systems. They influence the movement and behavior of organisms, the ecological interactions between and across populations, and the trophic structure of marine food webs. However, relative to their terrestrial equivalents, the wider ecological and economic importance of marine infochemicals remains understudied and a concerted, cross‐disciplinary effort is needed to reveal the full potential of marine chemical ecology. We highlight current challenges with specific examples and suggest how research on the chemical ecology of marine organisms could provide opportunities for implementing new management solutions for future “blue growth” (the sustainable use of ocean resources) and maintaining healthy marine ecosystems.

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Copepods drive large-scale trait-mediated effects in marine plankton

Abstract: Alarm signals from marine zooplankton structure phytoplankton communities.

Cited by 80 publications

References 32 publications

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

Transcriptomic responses to grazing reveal the metabolic pathway leading to the biosynthesis of domoic acid and highlight different defense strategies in diatoms

Chemical Signaling in the Turbulent Ocean—Hide and Seek at the Kolmogorov Scale

Using chemical language to shape future marine health

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