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Interactions of Vibrio Spp. with Zooplankton

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Interactions of Vibrio Spp. with Zooplankton Interactions of Vibrio spp. with Zooplankton MARTINA ERKEN,1 CARLA LUTZ,2 and DIANE McDOUGALD3 1Center for Marine Bio-Innovation, School of Biotechnology and Biomolecular Science, University of New South Wales, Sydney, NSW 2052, Australia; 2Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University, Singapore; 3ithree Institute, University of Technology, Sydney, Australia; and Singapore Centre on Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Singapore; and Center for Marine Bio-Innovation, School of Biotechnology and Biomolecular Science, University of New South Wales, Sydney, NSW 2052, Australia ABSTRACT Members of the genus Vibrio are known to associations being benign or beneficial, the majority of interact with phyto- and zooplankton in aquatic environments. current research usually focuses on pathogenic Vibrio These interactions have been proven to protect the bacterium spp. For example, Vibrio parahaemolyticus, Vibrio from various environmental stresses, serve as a nutrient source, vulnificus, and V. cholerae cause severe human diseases facilitate exchange of DNA, and to serve as vectors of disease transmission. This review highlights the impact of Vibrio- such as diarrhea, septicemia, and cholera (e.g., 14, 15, zooplankton interactions at the ecosystem scale and the 16), while Vibrio coralliilyticus and Vibrio tubiashii are importance of studies focusing on a wide range of causative agents of disease in commercially and ecolog- Vibrio-zooplankton interactions. The current knowledge on ically important organisms such as oysters and corals chitin utilization (i.e., chemotaxis, attachment, and degradation) (e.g., 17, 18). and the role of these factors in attachment to nonchitinous As common bacterioplankton in aquatic environ- zooplankton is also presented. ments, Vibrio spp. interact with planktonic animals (zooplankters) of many different phylogenetic affilia- INTRODUCTION tions and with different surface characteristics and com- positions. The numerous adaptations that have evolved Bacteria in the genus Vibrio are natural inhabitants of in Vibrio spp. that allow for surface colonization and aquatic environments. They are found in freshwater, intracellular associations with individual zooplankters estuarine and marine environments and are present in reflect the diversity of zooplankton. The best-studied the benthos and in the water column. As a result, Vibrio association of a Vibrio sp. with zooplankters is that spp. interact with higher organisms within the aquatic of V. cholerae and crustaceans such as copepods. The biosphere. Interactions of Vibrio spp. with representa- role of zooplankton in cholera transmission is well tives of the zooplankton community are of particular established, as is the role of chitin as a carbon source interest as these zooplankton have been proven to pro- for Vibrio spp. in the oligotrophic environment of the tect attached Vibrio spp. from various environmental oceans (e.g., 4, 19, 20, 21). stresses, serve as a nutrient source, facilitate exchange of DNA, and to serve as vectors of disease transmission Received: 14 October 2014, Accepted: 25 February 2015, (e.g., 1, 2, 3, 4, 5). Published: 29 May 2015 Editor: Michael Sadowsky, University of Minnesota, St. Paul, MN Vibrio spp. have been found to be associated with Citation: Erken M, Lutz C, McDougald D. 2015. Interactions of vibrio many higher organisms including fish (6), corals (7), spp. with zooplankton. Microbiol Spectrum 3(3):VE-0003-2014. sponges (8), hydroids (9), crabs (10), mollusks (11), and doi:10.1128/microbiolspec.VE-0003-2014. protozoa (12) (for a review of reservoirs for Vibrio Correspondence: Diane McDougald, [email protected] © 2015 American Society for Microbiology. All rights reserved. cholerae see reference 13). Despite the majority of these ASMscience.org/MicrobiolSpectrum 1 Downloaded from www.asmscience.org by IP: 200.55.51.2 On: Fri, 10 Jul 2015 17:28:57 Erken et al. To understand better which environmental factors competition and predation shape the planktonic com- promote the persistence of these microorganisms in munity from the smallest viruses to larger organisms the environment, it is necessary to understand their (such as jellyfish or cladocerans) and also impact the ecological niche, including interactions/adaptations that larger nekton communities (organisms that can swim may lead to disease events. In this review, we present against the current). All planktonic bacteria recycle nu- current knowledge on the interactions of Vibrio spp. trients by feeding on dissolved and particulate organic with higher organisms. We also review the impact of matter (DOM and POM, respectively) from exudates of Vibrio-zooplankton interactions at the ecosystem scale phytoplankton, nutrients released by “sloppy feeding” and highlight the importance of studies focusing on a of predators or exoskeletons of chitinous zooplankton wide range of Vibrio-zooplankton interactions, with a (24)(Fig. 1). Many bacteria, including most Vibrio spp., focus on recently published studies (within the last are chitinolytic, that is, they are able to obtain their 5 years). The current knowledge on chitin utilization nitrogen (N) and carbon (C) by degradation of chitin (i.e., chemotaxis, attachment, and degradation) and the (2, 25). role of these factors in attachment to nonchitinous The term zooplankton includes a large collection zooplankton is also presented. of heterotrophic groups, including but not limited to crustaceans such as copepods, water fleas (Daphnia spp.) and brine shrimp (e.g., Artemia spp.), nauplius ECOLOGICAL INTERACTIONS OF larvae, rotifers, heterotrophic protists, and jellyfish VIBRIO SPP. WITH ZOOPLANKTON (Fig. 2). Freshwater, coastal, and marine water zoo- The interactions of zooplankton and Vibrio spp. on a plankton communities differ in some respects but most global and/or ecosystem scale are influenced by many zooplankton taxa appear everywhere, just in different different abiotic and biotic factors such as temperature, abundances (22). The most important zooplankters in salinity, nutrients, and competing or predatory orga- these environments are protists and crustaceans such nisms. Just as Vibrio spp. have different niche prefer- as copepods and cladocerans. Many invertebrates, such ences, there are many zooplankters that, although they as annelids and chaetognaths, and the larvae of fish, share certain characteristics, occupy very diverse niches. echinoderms, mollusks, and arthropods, are also abun- To begin to understand the complex and diverse in- dant members of the zooplankton community. teractions of zooplankters and Vibrio spp. it is impor- The smallest representatives of the zooplankton tant to identify the different groups that comprise the community are flagellates, amoebae, and ciliates. These zooplankton. heterotrophic protists, or protozoa, are an important part of the planktonic community (Fig. 2D). These uni- Zooplankton Taxa cellular, eukaryotic organisms are essential components Plankton are biota suspended in a water body and of the microbial loop, and thus, are necessary for nu- although some are able to swim, they are not able to trient recycling and for controlling and shaping bacterial move against water currents (22). In general, plankton abundances in pelagic environments (26). Vibrio spp. consists of microscopic to macroscopic organisms of all have been shown to interact with flagellates, ciliates trophic levels. Their sizes range from the micrometer and amoebae in attached as well as in suspended com- scale to centimeters. Plankton includes organisms as munities (e.g., 12, 27, 28, 29, 30, 31). small as phages and other viruses (<0.2 μm, femto- Representatives of the phylum Rotifera are found plankton), bacteria (0.2 to 2 μm, picoplankton), and mostly in freshwater environments, with some occurring nano-flagellates (2 to 20 μm, nanoplankton). Larger in brackish water and only 100 taxa that are exclusively plankters include flagellates and ciliates (20 to 200 μm, marine (Fig. 2E)(22). These small (100 to 500 μm) meta- microplankton), rotifers, nauplii larvae, fish larvae, and zoans prey on protozoans, bacteria, yeasts and micro- copepods and cladocerans (0.2 to 20 mm, mesoplank- algae and they are themselves preyed upon by larger ton) of which many are visible to the naked eye (23). All plankton (32). Brachionus spp. play an important role in planktonic organisms that are able to carry out photo- Vibrio spp. ecology in Bangladesh, where the presence of synthesis to generate energy, such as autotrophic protists this rotifer was significantly correlated with the presence and cyanobacteria, are referred to as phytoplankton. of toxigenic strains of V. cholerae and with outbreaks of These planktonic communities are interconnected by cholera (33). complex and diverse bottom-up and top-down controls. Representatives of the phylum Arthropoda are the Nutrient availability, temperature, intra- and interspecies most abundant taxa of the zooplankton. Although 2 ASMscience.org/MicrobiolSpectrum Downloaded from www.asmscience.org by IP: 200.55.51.2 On: Fri, 10 Jul 2015 17:28:57 Interactions of Vibrio spp. with Zooplankton FIGURE 1 Food web interactions of planktonic organisms. Bacteria take up dissolved and particular organic matter (DOM and POM, respectively). Heterotrophic protists ingest bacteria within the planktonic environment and are themselves preyed upon by larger predatory protists and metazoans. Carcasses and fecal
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