Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

doi:10.1146/ANNUREV.MARINE.010908.163708

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Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

Journal Article•DOI•

Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems.

Mark E. Hay¹•Institutions (1)

Georgia Institute of Technology¹

25 Mar 2009-Annual Review of Marine Science (Annual Reviews)-Vol. 1, Iss: 1, pp 193-212

TL;DR: How chemical cues regulate critical aspects of the behavior of marine organisms from bacteria to phytoplankton to benthic invertebrates and water column fishes is reviewed.

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Abstract: Chemical cues constitute much of the language of life in the sea. Our understanding of biotic interactions and their effects on marine ecosystems will advance more rapidly if this language is studied and understood. Here, I review how chemical cues regulate critical aspects of the behavior of marine organisms from bacteria to phytoplankton to benthic invertebrates and water column fishes. These chemically mediated interactions strongly affect population structure, community organization, and ecosystem function. Chemical cues determine foraging strategies, feeding choices, commensal associations, selection of mates and habitats, competitive interactions, and transfer of energy and nutrients within and among ecosystems. In numerous cases, the indirect effects of chemical signals on behavior have as much or more effect on community structure and function as the direct effects of consumers and pathogens. Chemical cues are critical for understanding marine systems, but their omnipresence and impact are inadequ...

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Journal Article•DOI•

Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules.

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Christina C. Roggatz¹, Mark Lorch¹, Jörg D. Hardege¹, David M. Benoit¹•Institutions (1)

University of Hull¹

01 Dec 2016-Global Change Biology

TL;DR: It is found that peptide signalling cues are susceptible to protonation in future pH conditions, which will alter their overall charge and structure, and structure and electrostatic properties important for receptor binding differ significantly between the peptide forms present today and the protonated signalling peptides likely to be dominating in future oceans.

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Abstract: Ocean acidification is a global challenge that faces marine organisms in the near future with a predicted rapid drop in pH of up to 0.4 units by the end of this century. Effects of the change in ocean carbon chemistry and pH on the development, growth and fitness of marine animals are well documented. Recent evidence also suggests that a range of chemically mediated behaviours and interactions in marine fish and invertebrates will be affected. Marine animals use chemical cues, for example, to detect predators, for settlement, homing and reproduction. But, while effects of high CO2 conditions on these behaviours are described across many species, little is known about the underlying mechanisms, particularly in invertebrates. Here, we investigate the direct influence of future oceanic pH conditions on the structure and function of three peptide signalling molecules with an interdisciplinary combination of methods. NMR spectroscopy and quantum chemical calculations were used to assess the direct molecular influence of pH on the peptide cues, and we tested the functionality of the cues in different pH conditions using behavioural bioassays with shore crabs (Carcinus maenas) as a model system. We found that peptide signalling cues are susceptible to protonation in future pH conditions, which will alter their overall charge. We also show that structure and electrostatic properties important for receptor binding differ significantly between the peptide forms present today and the protonated signalling peptides likely to be dominating in future oceans. The bioassays suggest an impaired functionality of the signalling peptides at low pH. Physiological changes due to high CO2 conditions were found to play a less significant role in influencing the investigated behaviour. From our results, we conclude that the change of charge, structure and consequently function of signalling molecules presents one possible mechanism to explain altered behaviour under future oceanic pH conditions.

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114 citations

Cites background from "Marine chemical ecology: chemical s..."

...organisms across the phylogenetic tree (Hay, 2009)....
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...Only a very limited number of signalling cue structures and their respective biological function have been identified so far (Hay, 2009)....
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...These signalling cues are as diverse as their biological functions and can be based on every form of biological molecule from amino acids to nucleic acids and carbohydrates (Hay, 2009; Wyatt, 2014a)....
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...In fact, peptides and amino acid-derived cues mediate a vast number of diverse behaviours that can affect species and communities and even have an impact at ecosystem level (Hay, 2009; Wyatt, 2014b)....
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...+44 1482 465457, e-mail: C.Roggatz@hull.ac.uk 3914 © 2016 John Wiley & Sons Ltd organisms across the phylogenetic tree (Hay, 2009)....
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Journal Article•DOI•

The Relevance of Marine Chemical Ecology to Plankton and Ecosystem Function: An Emerging Field

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Adrianna Ianora¹, Matthew G. Bentley, Gary S. Caldwell, Raffaella Casotti, Allan Cembella, Jonna Engström-Öst, Claudia Halsband, Eva C. Sonnenschein², Catherine Legrand, Carole A. Llewellyn, Aistë Paldavičienë, Renata Pilkaityte, Georg Pohnert, Arturas Razinkovas, Giovanna Romano, Urban Tillmann, Diana Vaiciute - Show less +13 more•Institutions (2)

Stazione Zoologica Anton Dohrn¹, Max Planck Society²

22 Sep 2011-Marine Drugs

TL;DR: This work focuses on bioactive compounds and interactions associated with phytoplankton, particularly bloom-forming diatoms, prymnesiophytes and dinoflagellates, and their effects on grazers.

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Abstract: Marine chemical ecology comprises the study of the production and interaction of bioactive molecules affecting organism behavior and function. Here we focus on bioactive compounds and interactions associated with phytoplankton, particularly bloom-forming diatoms, prymnesiophytes and dinoflagellates. Planktonic bioactive metabolites are structurally and functionally diverse and some may have multiple simultaneous functions including roles in chemical defense (antipredator, allelopathic and antibacterial compounds), and/or cell-to-cell signaling (e.g., polyunsaturated aldehydes (PUAs) of diatoms). Among inducible chemical defenses in response to grazing, there is high species-specific variability in the effects on grazers, ranging from severe physical incapacitation and/or death to no apparent physiological response, depending on predator susceptibility and detoxification capability. Most bioactive compounds are present in very low concentrations, in both the producing organism and the surrounding aqueous medium. Furthermore, bioactivity may be subject to synergistic interactions with other natural and anthropogenic environmental toxicants. Most, if not all phycotoxins are classic secondary metabolites, but many other bioactive metabolites are simple molecules derived from primary metabolism (e.g., PUAs in diatoms, dimethylsulfoniopropionate (DMSP) in prymnesiophytes). Producing cells do not seem to suffer physiological impact due to their synthesis. Functional genome sequence data and gene expression analysis will provide insights into regulatory and metabolic pathways in producer organisms, as well as identification of mechanisms of action in target organisms. Understanding chemical ecological responses to environmental triggers and chemically-mediated species interactions will help define crucial chemical and molecular processes that help maintain biodiversity and ecosystem functionality.

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114 citations

Cites background or result from "Marine chemical ecology: chemical s..."

...In contrast to the relatively well-studied chemical interactions between benthic plant metabolites and herbivores [5], the effects of microbial secondary metabolites on planktonic herbivores are not well known and remain under-investigated....
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...be low and may be compensated for by the benefit of reduced predation risk [5]....
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Journal Article•DOI•

Synergistic allelochemicals from a freshwater cyanobacterium.

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Pedro N. Leão¹, Alban R. Pereira, Wei-Ting Liu, Julio Ng, Pavel A. Pevzner, Pieter C. Dorrestein, Gabriele M. König, Vitor Vasconcelos, William H. Gerwick - Show less +5 more•Institutions (1)

University of Porto¹

22 Jun 2010-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: It is observed that maximal allelopathic activity is highest in early growth stages of the cyanobacterium, and this provided sufficient material for isolation and chemical characterization of active compounds that inhibited the growth of C. vulgaris.

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Abstract: The ability of cyanobacteria to produce complex secondary metabolites with potent biological activities has gathered considerable attention due to their potential therapeutic and agrochemical applications. However, the precise physiological or ecological roles played by a majority of these metabolites have remained elusive. Several studies have shown that cyanobacteria are able to interfere with other organisms in their communities through the release of compounds into the surrounding medium, a phenomenon usually referred to as allelopathy. Exudates from the freshwater cyanobacterium Oscillatoria sp. had previously been shown to inhibit the green microalga Chlorella vulgaris. In this study, we observed that maximal allelopathic activity is highest in early growth stages of the cyanobacterium, and this provided sufficient material for isolation and chemical characterization of active compounds that inhibited the growth of C. vulgaris. Using a bioassay-guided approach, we isolated and structurally characterized these metabolites as cyclic peptides containing several unusually modified amino acids that are found both in the cells and in the spent media of Oscillatoria sp. cultures. Strikingly, only the mixture of the two most abundant metabolites in the cells was active toward C. vulgaris. Synergism was also observed in a lung cancer cell cytotoxicity assay. The binary mixture inhibited other phytoplanktonic organisms, supporting a natural function of this synergistic mixture of metabolites as allelochemicals.

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113 citations

Journal Article•DOI•

Reduced pH sea water disrupts chemo-responsive behaviour in an intertidal crustacean

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Kate L. de la Haye¹, John I. Spicer¹, Stephen Widdicombe², Mark Briffa¹•Institutions (2)

University of Plymouth¹, Plymouth Marine Laboratory²

31 Jan 2012-Journal of Experimental Marine Biology and Ecology

TL;DR: This study shows that the chemo-responsiveness of a crustacean may be influenced by both naturally occurring pH fluctuations and future anthropogenically-induced changes in ocean pH.

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112 citations

Additional excerpts

...(Hay, 2009; Lima and Dill, 1990; Wisenden, 2000)....
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Journal Article•DOI•

Reduced sea water pH disrupts resource assessment and decision making in the hermit crab Pagurus bernhardus

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K.L. de la Haye¹, John I. Spicer¹, Steve Widdicombe², Mark Briffa¹•Institutions (2)

University of Plymouth¹, Plymouth Marine Laboratory²

01 Sep 2011-Animal Behaviour

TL;DR: A reduction in sea water pH disrupts the resource assessment and decision-making processes of hermit crabs, indicating that the ability to acquire a vital resource may be influenced by both naturally occurring environmental cycles and anthropogenically induced environmental change.

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106 citations

Cites background from "Marine chemical ecology: chemical s..."

...Given the importance of chemical cues in the marine environment, any disruption to chemosensory behaviour could have serious consequences for community dynamics (Atema 1995; Hay 2009)....
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...de la Haye et al. / Animal Behaviour 82 (2011) 495e501 496...
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References

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Journal Article•

Chemical ecology of the settlement of benthic marine invertebrates

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Joseph R. Pawlik

01 Jan 1992-Oceanography and Marine Biology

839 citations

"Marine chemical ecology: chemical s..." refers background in this paper

...…to chemical cues from specific hosts, or corals that settle in response to chemical traits of specific crustose coralline algae, or of soft-substrate animals that recruit to or avoid sands treated with specific chemical cues or extracts (e.g., Pawlik 1992, Krug & Manzi 1999, Hadfield & Paul 2001)....
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...In aquatic systems, chemical cues determine feeding, habitat, and mating choices (e.g., Hay & Fenical 1988, 1996; Pawlik 1992; Breithaupt & Thiel 2008)....
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...…stimulating feeding once prey have been contacted; compounds responsible for attraction from a distance have rarely been investigated for adult specialist consumers [compounds that cue larval settlement have been investigated; see Pawlik (1992), Krug & Manzi (1999), and Hadfield & Paul (2001)]....
[...]

Journal Article•DOI•

Centuries of Human-Driven Change in Salt Marsh Ecosystems

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K. Bromberg Gedan¹, Brian R. Silliman¹, Mark D. Bertness²•Institutions (2)

Brown University¹, University of Florida²

25 Mar 2009-Annual Review of Marine Science

TL;DR: It is concluded that the best way to protect salt marshes and the services they provide is through the integrated approach of ecosystem-based management.

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Abstract: Salt marshes are among the most abundant, fertile, and accessible coastal habitats on earth, and they provide more ecosystem services to coastal populations than any other environment. Since the Middle Ages, humans have manipulated salt marshes at a grand scale, altering species composition, distribution, and ecosystem function. Here, we review historic and contemporary human activities in marsh ecosystems—exploitation of plant products; conversion to farmland, salt works, and urban land; introduction of non-native species; alteration of coastal hydrology; and metal and nutrient pollution. Unexpectedly, diverse types of impacts can have a similar consequence, turning salt marsh food webs upside down, dramatically increasing top down control. Of the various impacts, invasive species, runaway consumer effects, and sea level rise represent the greatest threats to salt marsh ecosystems. We conclude that the best way to protect salt marshes and the services they provide is through the integrated approach of ecosystem-based management.

...read moreread less

770 citations

Journal Article•DOI•

Marine Plant-Herbivore Interactions: The Ecology of Chemical Defense

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Mark E. Hay, William Fenical

01 Jan 1988-Annual Review of Ecology, Evolution, and Systematics

TL;DR: Although numerous seaweed characteristics can deter some herbivores, the effects of morphology and chemistry have been studied most thoroughly and these types of seaweeds may be considered herbivore tolerant.

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Abstract: Herbivory has a profound effect on seaweeds in both temperate and tropical communities (11, 17, 21, 33, 43, 47, 80, 124). This is especially true on coral reefs where 60-97% (11, 42) of the total seaweed production may be removed by herbivores. To persist in marine communities, seaweeds must escape, deter, or tolerate herbivory. The ecological and evolutionary importance of spatial and temporal escapes has been extensively studied for seaweeds and adequately reviewed in the recent literature (33, 45, 47, 71, 80). The ability of seaweeds to tolerate herbivory has received limited attention. On coral reefs, rapidly growing filamentous algae are heavily grazed, but the algae quickly replace these losses and appear to be dependent upon herbivores to prevent their habitat from being overgrown by larger but less herbivoretolerant species (11, 71). Additionally, several seaweeds have spores or vegetative portions that can withstand gut passage; in some cases this significantly increases the growth rates of the newly settled spores (6, 122). These types of seaweeds may be considered herbivore tolerant. Although numerous seaweed characteristics can deter some herbivores, the effects of morphology and chemistry have been studied most thoroughly. The

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722 citations

"Marine chemical ecology: chemical s..." refers background in this paper

...In aquatic systems, chemical cues determine feeding, habitat, and mating choices (e.g., Hay & Fenical 1988, 1996; Pawlik 1992; Breithaupt & Thiel 2008)....
[...]
...…on the plants they consume and that are especially susceptible to predation suggest that feeding preferences are commonly driven by the need to colonize hosts that provide escapes from consumers rather than by the direct food value of those hosts (see also Hay & Fenical 1988, 1996; Hay 1992, 1996)....
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...In the past 20 years, the review of selected aspects of marine chemical ecology has become a growth industry (e.g., Hay & Fenical 1988, 1996; Paul 1992; Hay 1996; McClintock & Baker 2001; Paul et al. 2007; Pohnert et al. 2007; Amsler 2008), with numerous reviews focusing on specific groups…...
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Journal Article•DOI•

Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein.

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Mike Manefield¹, Rocky de Nys¹, Kumar Naresh¹, Read Roger¹, Michael Givskov², Steinberg Peter¹, Staffan Kjelleberg¹ - Show less +3 more•Institutions (2)

University of New South Wales¹, Technical University of Denmark²

01 Feb 1999-Microbiology

TL;DR: The contention that furanones, at the concentrations produced by the alga, can control bacterial colonization of surfaces by specifically interfering with AHL-mediated gene expression at the level of the LuxR protein is supported.

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Abstract: Summary: Acylated homoserine lactone (AHL)-mediated gene expression controls phenotypes involved in colonization, often specifically of higher organisms, in both marine and terrestrial environments. The marine red alga Delisea pulchra produces halogenated furanones which resemble AHLs structurally and show inhibitory activity at ecologically realistic concentrations in AHL bioassays. Evidence is presented that halogenated furanones displace tritiated OHHL [N-3- (oxohexanoy1)-L-homoserine lactone] from Escherichia coli cells overproducing LuxR with potencies corresponding to their respective inhibitory activities in an AHL-regulated bioluminescence assay, indicating that this is the mechanism by which furanones inhibit AHL-dependent phenotypes. Alternative mechanisms for this phenomenon are also addressed. General metabolic disruption was assessed with two-dimensional PAGE, revealing limited non- AHL-related effects. A direct chemical interaction between the algal compounds and AHLs, as monitored by 1H NMR spectroscopy, was shown not to occur in vitro. These results support the contention that furanones, at the concentrations produced by the alga, can control bacterial colonization of surfaces by specifically interfering with AHL-mediated gene expression at the level of the LuxR protein.

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612 citations

"Marine chemical ecology: chemical s..." refers background in this paper

...This inhibition occurs because halogenated furanones interfere with the bacteria’s signal-based regulatory systems that control surface motility, exoenzyme production, and biofilm formation/stability (Manefield et al. 1999, 2002; Rasmussen et al. 2000; McDougald et al. 2001)....
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Journal Article•DOI•

Marine chemical ecology: what's known and what's next?

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Mark E. Hay¹•Institutions (1)

University of North Carolina at Chapel Hill¹

15 Nov 1996-Journal of Experimental Marine Biology and Ecology

TL;DR: This review concludes that relatively unstudied, ontogenetic shifts in concentrations and types of defenses occur in marine species, and patterns of larval chemical defenses appear to provide insights into the evolution of complex life cycles and of differing modes of development among marine invertebrates.

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607 citations

"Marine chemical ecology: chemical s..." refers background in this paper

...…on the plants they consume and that are especially susceptible to predation suggest that feeding preferences are commonly driven by the need to colonize hosts that provide escapes from consumers rather than by the direct food value of those hosts (see also Hay & Fenical 1988, 1996; Hay 1992, 1996)....
[...]
...In other instances the larvae are chemically defended, but the adults are not and appear instead to rely more on physical/structural defenses (Lindquist & Hay 1996)....
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...…past 20 years, the review of selected aspects of marine chemical ecology has become a growth industry (e.g., Hay & Fenical 1988, 1996; Paul 1992; Hay 1996; McClintock & Baker 2001; Paul et al. 2007; Pohnert et al. 2007; Amsler 2008), with numerous reviews focusing on specific groups (seaweeds…...
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...Once larvae or embryos are released from brooding adults, they can be at considerable risk of predation in the plankton, but even more so as they recruit to the benthos where both fish and invertebrate predators are commonly concentrated (Lindquist & Hay 1996)....
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...…of resistance to host chemical defenses, selective consumption of those hosts, being cued to feed by the specific host chemicals that deter other consumers, and sequestration by the specialist of its host’s chemical defenses, thus becoming immune to many of its own enemies (Hay 1992, 1996)....
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