The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts

The activities of unicellular microbes dominate the ecology of the marine environment, but the chemical signals that determine behavioral interactions are poorly known. In particular, chemical signals between microbial predators and prey contribute to food selection or avoidance and to defense, factors that probably affect trophic structure and such large-scale features as algal blooms. Using defense as an example, I consider physical constraints on the transmission of chemical information, and strategies and mechanisms that microbes might use to send chemical signals. Chemical signals in a low Re, viscosity-dominated physical environment are transferred by molecular diffusion and laminar advection, and may be perceived at nanomolar levels or lower. Events that occur on small temporal and physical scales in the "near-field" of prey are likely to play a role in cell-cell interactions. On the basis of cost-benefit optimization and the need for rapid activation, I suggest that microbial defense system strategies might be highly dynamic. These strategies include compartmented and activated reactions, utilizing both pulsed release of dissolved signals and contact-activated signals at the cell surface. Bioluminescence and extrusome discharge are two visible manifestations of rapidly activated microbial defenses that may serve as models for other chemical reactions as yet undetected due to the technical problems of measuring transient chemical gradients around single cells. As an example, I detail an algal dimethylsulfoniopropionate (DMSP) cleavage reaction that appears to deter protozoan feeding and explore it as a possible model for a rapidly activated, short-range chemical defense system. Although the exploration of chemical interactions among planktonic microbes is in its infancy, ecological models from macroorganisms provide useful hints of the complexity likely to be found.     

Role of planktonic and sessile extracellular metabolic byproducts on <Emphasis Type="Italic">Pseudomonas aeruginosa</Emphasis> and <Emphasis Type="Italic">Escherichia coli</Emphasis> intra and interspecies relationships

Bacterial species are found primarily as residents of complex surface-associated communities, known as biofilms. Although these structures prevail in nature, bacteria still exist in planktonic lifestyle and differ from those in morphology, physiology, and metabolism. This study aimed to investigate the influence of physiological states of Pseudomonas aeruginosa and Escherichia coli in cell-to-cell interactions. Filtered supernatants obtained under planktonic and biofilm cultures of each single species were supplemented with tryptic soy broth (TSB) and used as the growth media (conditioned media) to planktonic and sessile growth of both single- and two-species cultures. Planktonic bacterial growth was examined through OD₆₄₀ measurement. One-day-old biofilms were evaluated in terms of biofilm biomass (CV), respiratory activity (XTT), and CFU number. Conditioned media obtained either in biofilm or in planktonic mode of life triggered a synergistic effect on planktonic growth, mainly for E. coli single cultures growing in P. aeruginosa supernatants. Biofilms grown in the presence of P. aeruginosa biofilms-derived metabolites presented less mass and activity. These events highlight that, when developed in biofilm, P. aeruginosa release signals or metabolites able to prejudice single and binary biofilm growth of others species and of their own species. However, products released by their planktonic counterparts did not impair biofilm growth or activity. E. coli, living as planktonic or sessile cultures, released signals and metabolites or removed un-beneficial compounds which promoted the growth and activity of all the species. Our findings revealed that inter and intraspecies behaviors depend on the involved bacteria and their adopted mode of life.     

A co-culturing/metabolomics approach to investigate chemically mediated interactions of planktonic organisms reveals influence of bacteria on diatom metabolism

Chemically mediated interactions are hypothesized to be essential for ecosystem functioning as co-occurring organisms can influence the performance of each other by metabolic means. A metabolomics approach can support a better understanding of such processes but many problems cannot be addressed due to a lack of appropriate co-culturing and sampling strategies. This is particularly true for planktonic organisms that live in complex but very dilute communities in the open water. Here we present a co-culturing device that allows culturing of microalgae and bacteria that are physically separated but can exchange dissolved or colloidal chemical signals. Identical growth conditions for both partners as well as high metabolite diffusion rates between the culturing chambers are ensured. This setup allowed us to perform a metabolomic survey of the effect of the bacterium Dinoroseobacter shibae on the diatom Thalassiosira pseudonana. GC–MS measurements revealed a pronounced influence of the bacterium on the metabolic profile of T. pseudonana cells with especially intracellular amino acids being up-regulated in co-cultures. Despite the influence on diatom metabolism, the bacterium has little influence on the growth of the algae. This might indicate that the observed metabolic changes represent an adaptive response of the diatoms. Such interactions might be crucial for metabolic fluxes within plankton communities.     

Chemical interactions in diatoms: role of polyunsaturated aldehydes and precursors

Chemicals produced by aquatic organisms, and especially micro-organisms, have received increasing attention in the last decade for their role in shaping interactions and communities. Several cases emphasize the fact that chemical signals or defence may modulate interspecific interactions. Notably, it has been shown that diatoms, unicellular algae and key primary producers in aquatic ecosystems produce a wide range of bioactive metabolites. Among these compounds, polyunsaturated short-chain aldehydes in vitro strongly impair the reproduction of various potential grazers. In the field, the relationship between aldehyde production and reproductive failure in copepods remains unclear. Recent studies have suggested that these putative defence compounds may also be involved in intercellular communication and in interactions with competitors. Potential effects of the aldehyde precursors on various organisms have also been described. This review presents an overview of various results obtained in the last decade that could help us to understand the role of polyunsaturated aldehydes and their precursors in the ecology of diatoms. It is focused on the dichotomy between freshwater and marine environments. Indeed, most of the results on anti-proliferative aldehydes concern marine planktonic diatoms, whereas they are also known to be produced by benthic and freshwater species.     

Effects of air pollution on biogenic volatiles and ecological interactions

Chemical signals play important roles in ecological interactions but are vulnerable to perturbation by air pollution. In polluted air masses, signals may travel shorter distances before being destroyed by chemical reactions with pollutants, thus losing their specificity. To determine which scent-mediated interactions are likely to be affected, we review existing literature to build a picture of what chemicals are commonly found in such interactions and the spatial scales at which interactions occur. We find that pollination, attraction of natural enemies of plant pests, aggregation pheromones, and mate attraction are likely to be affected. We review the scant literature on this topic and extend the hypothesis to include heretofore unexplored interactions. New research should investigate whether air pollution deleteriously affects populations of organisms that rely on scent plumes. Additionally, we need to investigate whether or not breakdown products created by the reaction of signaling chemicals with pollutants can provide usable signals, and whether or not there has been adaptation on the part of scent emitters or receivers to use either breakdown products or more robust chemical signals. The proposed research will necessarily draw on tools from atmospheric science, evolutionary biology, and ecology in furthering our understanding of the ecological implications of how air pollution modifies the scentscape.     

Receptor-receptor interactions as an integrative mechanism in nerve cells

Several lines of evidence indicate that interactions among transmission lines can take place at the level of the cell membrane via interactions among macromolecules, integral or associated to the cell membrane, involved in signal recognition and transduction. The present view will focus on this last subject, i.e., on the interactions between receptors for chemical signals at the level of the neuronal membrane (receptor-receptor interaction). By receptor-receptor interaction we mean that a neurotransmitter or modulator, by binding to its receptor, modifies the characteristics of the receptor for another transmitter or modulator. Four types of interactions among transmission lines may be considered, but mainly intramembrane receptor-receptor interactions have been dealt with in this article, exemplified by the heteroregulation of D2 receptors via neuropeptide receptors and A2 receptors. The role of receptor-receptor interactions in the integration of signals is discussed, especially in terms of filtration of incoming signals, of integration of coincident signals, and of neuronal plasticity.     

The effect of the chemical environment on interactions in groups of crayfish

Most of our knowledge of social behaviour in crustaceans stems from observations of pairs of animals engaged in conflict. Less consideration has been given to the dynamics of group behaviour. We investigated whether chemical signals affect the dynamic of groups of Cherax destructor. Animals were exposed to odours collected from male, female, moulted or dominant crayfish, or from fish. We observed agonistic encounters in the group during a 15 min period after the introduction of the odour. There was a decrease in threat behaviours when the male odour was added. We conclude from this that an olfactory stimulus can affect the dynamic of group interactions and the results suggest that the outcome is likely to be different from that obtained with paired or single individuals.     

Chemical information transfer in freshwater plankton

The structure of aquatic ecosystems is determined by complex interactions among individual organisms at different trophic levels. Although our basic understanding of how top-down and bottom-up processes interact to determine food-web dynamics has advanced, we still lack insights into how complex interactions and feedbacks affect the dynamics and structure of food webs. It is now becoming increasingly clear that, in addition to energy transfer from one trophic level to the other, there is exchange of information between these levels facilitated by the release of infochemicals by the organisms. There is evidence from recent studies that the exchange of chemical information in freshwater ecosystems is likely to play a decisive role in shaping structure and functioning of these systems. Chemical communication among freshwater organisms mediates many aspects of both predation and interspecific competition, which play key roles in determining community structure and ecosystem functioning. For example, consumer-induced defences in phytoplankton and zooplankton include modifications in the characteristics relating to life history, behaviour, morphology and biochemistry. These inducible defences affect trophic interactions by altering predator feeding rates through changes in attack rate or handling time, or both. Also host-specific fungal parasitism in phytoplankton is probably controlled by infochemicals. The motile fungi recognise their host by host-secreted compounds. Until now models describing the functioning of ecosystems mainly considered flows of biomass and energy. Integration of new knowledge about the role of chemical communication in these models may be one of the aims of ecological informatics. In this chapter I discuss how infochemicals may affect the dynamics and structure of planktonic food webs.     

植物化学通讯研究进展

 生物的信息传递是生命科学中引人入胜的研究领域之一,生物种间种内和个体内都存在着物理和化学等各种信息交流方式。植物种间种内是否通过物理信号进行通讯交流还是一个未知数,但邻近的同种或异种植物通过化学物质为媒介的通讯关系确是客观存在的。最近,愈来愈多的研究证明：许多陆生植物种可以合成并释放特定的次生物质,这些次生物质可以通过空气和土壤两种载体进行信息传递,尤其是在植物受到侵袭和寄生条件下。茉莉酮酸甲酯、水杨酸甲酯和乙烯等挥发性次生物质被确证为以空气为媒介进行植物种间和种内通讯的化学信号分子。植物根分泌的黄酮和氢醌等分子也可以经土壤媒介传递信息。由于在自然条件下植物根系分泌物的收集和活性信号分子的俘获及鉴定技术还未能突破,这增加了以土壤为媒介的植物种间和种内化学通讯关系研究的难度。但不论如何,植物的化学通讯是植物种间和种内交流的主要方式,植物间的化学通讯关系的研究还处于突破的前夜,这方面的任一研究成果都会引起世界性的关注。因此,破译植物种间和种内化学通讯密码具有重要的学术价值。     

Social context influences chemical communication in D. melanogaster males

Chemical communication mediates social interactions in insects. For the fruit fly, D. melanogaster, the chemical display is a key fitness trait because it leads to mating. An exchange of cues that resembles a dialogue between males and females is enacted by pheromones, chemical signals that pass between individual flies to alter physiology and behavior. Chemical signals also affect the timing of locomotor activity and sleep. We investigated genetic and environmental determinants of chemical communication. To evaluate the role of the social environment, we extracted a chemical blend from individual males selected from groups composed of one genotype and compared these extracts to those from groups of mixed genotypes. To evaluate the role of the physical environment, these comparisons were performed under a light-dark cycle or in constant darkness. Here, we show that chemical signaling is affected by the social environment, light-dark cycle, and genotype as well as the complex interplay of these variables. Gene-by-environment interactions produce highly significant effects on chemical signaling. We also examined individual responses within the groups. Strikingly, the response of one wild-type fly to another is modulated by the genotypic composition of his neighbors. Chemical signaling in D. melanogaster may be a "fickle" trait that depends on the individual's social background.     

Chemical interactions between planktonic crustaceans

Three levels of chemical communications involved plankton Crustacea are considered: 1) Influence of zooplankton excretion on phytoplankton; 2) Influence of zooplankton excretion on the individuals of the same or other species of the same trophic level; 3) Influence of chemical cues released by predatory zooplankton and fish on herbivorous zooplankton. The data on the influence of excreted cues on some physiological (growth, reproduction, feeding, etc.) and behavioural (vertical and horizontal migrations) characters of planktonic crustaceans are presented. Ecological role and chemistry cues responsible for the interactions of different trophic levels can be different. It is considered that chemical communications in aquatic ecosystems can be provided with: 1) Species-specific cues that strictly influence particular biological functions (communication system of feromone type); 2) Non-specific cues that strictly influence particular functions (system of regulator, that act at the whole ecosystem as the hormonal system of an organism). 3) Non-specific substances with broad (non-specidic) influence--toxic substances of "biocondition substances" according to classification of Novikov and Kharlamova (2000).     

Communication in bacteria: an ecological and evolutionary perspective

Individual bacteria can alter their behaviour through chemical interactions between organisms in microbial communities - this is generally referred to as quorum sensing. Frequently, these interactions are interpreted in terms of communication to mediate coordinated, multicellular behaviour. We show that the nature of interactions through quorum-sensing chemicals does not simply involve cooperative signals, but entails other interactions such as cues and chemical manipulations. These signals might have a role in conflicts within and between species. The nature of the chemical interaction is important to take into account when studying why and how bacteria react to the chemical substances that are produced by other bacteria.     

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

Recent insights about relationships between nutrient availability,forms, and stoichiometry,and the distribution,ecophysiology, and food web effects of pelagic and benthic Prorocentrum species

The genus Prorocentrum includes six planktonic species that form high-biomass blooms, and at least nine predominantly benthic toxigenic species. Four of the plankters, including P. minimum, the only plankter reported to be toxigenic, are among the most commonly recognized harmful algae that are increasing in frequency, duration, and magnitude globally. Culture studies suggest a species group that generally grows maximally at inorganic nutrient N:P ratios just below Redfield proportions. However, field studies indicate that planktonic Prorocentrum species bloom when nutrients are at high N:P ratios relative to Redfield proportions. In the benthic species P. lima complex, toxin production has been shown to be inversely related to nutrient limitation, increasing when nutrient ratios are above Redfield proportions. Mixotrophy and allelopathy can play an important role in the interactions among planktonic Prorocentrum species, diatoms and other dinoflagellates, but little information is available for benthic taxa. The available information suggests that there are allelopathic interactions among benthic species and other algae, and that benthic species also can adversely affect finfish and shellfish health. While high growth rates may allow these plankters to initiate blooms, adaptive physiology is hypothesized to allow blooms to be maintained at less than maximal growth rates and at non-optimal N:P ratios. Given the projection for land-based nutrient export to continue to increase, it is expected that there will be further expansion of planktonic harmful Prorocentrum spp. globally and more intensive or more toxic benthic occurrences in the future.     

The effect of habitat structure on prey mortality depends on predator and prey microhabitat use

Structurally complex habitats provide cover and may hinder the movement of animals. In predator–prey relationships, habitat structure can decrease predation risk when it provides refuges for prey or hinders foraging activity of predators. However, it may also provide shelter, supporting structures and perches for sit-and-wait predators and hence increase their predation rates. We tested the effect of habitat structure on prey mortality in aquatic invertebrates in short-term laboratory predation trials that differed in the presence or absence of artificial vegetation. The effect of habitat structure on prey mortality was context dependent as it changed with predator and prey microhabitat use. Specifically, we observed an ‘anti-refuge’ effect of added vegetation: phytophilous predators that perched on the plants imposed higher predation pressure on planktonic prey, while mortality of benthic prey decreased. Predation by benthic and planktonic predators on either type of prey remained unaffected by the presence of vegetation. Our results show that the effects of habitat structure on predator–prey interactions are more complex than simply providing prey refuges or cover for predators. Such context-specific effects of habitat complexity may alter the coupling of different parts of the ecosystem, such as pelagic and benthic habitats, and ultimately affect food web stability through cascading effects on individual life histories and trophic link strengths.     

Closing the larval loop: linking larval ecology to the population dynamics of marine benthic invertebrates

The majority of marine benthic invertebrates exhibit a complex life cycle that includes separate planktonic larval, and bottom-dwelling juvenile and adult phases. To understand and predict changes in the spatial and temporal distributions, abundances, population growth rate, and population structure of a species with such a complex life cycle, it is necessary to understand the relative importance of the physical, chemical and biological properties and processes that affect individuals within both the planktonic and benthic phases. To accomplish this goal, it is necessary to study both phases within a common, quantitative framework defined in terms of some common currency. This can be done efficiently through construction and evaluation of a population dynamics model that describes the complete life cycle.

Two forms that such a model might assume are reviewed: a stage-based, population matrix model, and a model that specifies discrete stages of the population, on the bottom and in the water column, in terms of simultaneous differential equations that may be solved in both space and time. Terms to be incorporated in each type of model can be formulated to describe the critical properties and processes that can affect populations within each stage of the life cycle. For both types of model it is shown how this might be accomplished using an idealized balanomorph barnacle as an example species. The critical properties and processes that affect the planktonic and benthic phases are reviewed. For larvae, these include benthic adult fecundity and fertilization success, growth and larval stage duration, mortality, larval behavior, dispersal by currents and turbulence, and larval settlement. It is possible to predict or estimate empirically all of the key terms that should be built into the larval and benthic components of the model. Thus, the challenge of formulating and evaluating a full life cycle model is achievable. Development and evaluation of such a model will be challenging because of the diverse processes which must be considered, and because of the disparities in the spatial and temporal scales appropriate to the benthic and planktonic larval phases. In evaluating model predictions it is critical that sampling schemes be matched to the spatial and temporal scales of model resolution.     

背角无齿蚌(Anodonta woodiana)对浅水系统底栖和浮游藻类竞争关系的影响

底栖藻类和浮游藻类之间的竞争关系对浅水生态系统的结构、功能具有重要的影响,双壳类可通过滤食控制浮游藻类,从而改变底栖藻类与浮游藻类之间的竞争结果。论文通过比较放养背角无齿蚌(Anodonta woodiana)(蚌处理组)与不放养背角无齿蚌(对照组)系统中底栖藻类、浮游藻类的生物量和优势种等的变化,研究了滤食性双壳类对底栖藻类和浮游藻类间竞争的影响。结果表明,背角无齿蚌可显著降低浮游藻类生物量,提高水体透明度和沉积物表面光照条件,从而显著提高底栖藻类的生物量;背角无齿蚌也改变了浮游藻类的优势种,使优势种由蓝藻转变成硅藻。因此,滤食性双壳类有利于促进浅水生态系统从混水态向清水态转变,本研究结果对富营养化浅水湖泊修复与管理具有一定的参考意义。     

Feeding In Planktonic Protozoans: Evidence For Non-Random Acquisition of Prey

ABSTRACT The literature on discriminant feeding by planktonic protozoans using geometric and nongeometric criteria is reviewed with emphasis on recent studies that indicate phagotrophic protists can use information other than particle size or shape to sort among potential prey. Sufficient data are available for ciliates, aplastidic microflagellates, and phagotrophic dinoflagellates. Numerous representative taxa of all three groups have chemosensory capabilities, either to specific chemicals or to prey exudates, that modify their motility patterns resulting in aggregation or dispersal. Representatives of all three groups also have specific prey preferences. These considerations imply, but do not prove, selectivity in feeding through use of chemical cues. Although prey geometry is clearly a first-order determinant of ingestion through passive mechanical selection, recent studies illustrate that planktonic ciliates and flagellates can use other criteria to discriminate among prey. the evidence clearly implicates use of chemical cues, most likely perceived through contact chemoreception. Filter feeders as well as raptors have such abilities indicating that feeding mechanisms per se do not imply limitations on feeding behavior. Evidence of considerable flexibility and complexity in chemoperceptive feeding suggests that we have only glimpsed the more detailed features of feeding behavior in aquatic protozoans.