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Cnidarian Interaction with Microbial Communities: from Aid to Animal’S Health to Rejection Responses

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Cnidarian Interaction with Microbial Communities: from Aid to Animal’S Health to Rejection Responses marine drugs Review Cnidarian Interaction with Microbial Communities: From Aid to Animal’s Health to Rejection Responses Loredana Stabili 1,2,* ID , Maria Giovanna Parisi 3, Daniela Parrinello 3 and Matteo Cammarata 3,* 1 Istituto per l’Ambiente Marino Costiero, U.O.S. di Taranto, CNR, Via Roma 3, 74123 Taranto, Italy 2 Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, via Prov.le Lecce Monteroni, 73100 Lecce, Italy 3 Laboratory of Marine Immunobiology, Dipartimento delle Scienze della Terra e del Mare, Università di Palermo, Viale delle Scienze Ed. 16, 90128 Palermo, Italy; [email protected] (M.G.P.); [email protected] (D.P.) * Correspondence: [email protected] (L.S.); [email protected] (M.C.) Received: 27 July 2018; Accepted: 16 August 2018; Published: 23 August 2018 Abstract: The phylum Cnidaria is an ancient branch in the tree of metazoans. Several species exert a remarkable longevity, suggesting the existence of a developed and consistent defense mechanism of the innate immunity capable to overcome the potential repeated exposure to microbial pathogenic agents. Increasing evidence indicates that the innate immune system in Cnidarians is not only involved in the disruption of harmful microorganisms, but also is crucial in structuring tissue-associated microbial communities that are essential components of the Cnidarian holobiont and useful to the animal’s health for several functions, including metabolism, immune defense, development, and behavior. Sometimes, the shifts in the normal microbiota may be used as “early” bio-indicators of both environmental changes and/or animal disease. Here the Cnidarians relationships with microbial communities and the potential biotechnological applications are summarized and discussed. Keywords: cnidarian; anthozoa; microbial communities; cnidarian holobiont; zooxanthellae; bleaching; antibacterial activity 1. Introduction to Cnidarian Cnidarian are a group made up of more than 9,000 living species, exclusively aquatic, getting their name from the presence of cnidocysts connected to supporting cells and neurons. These in turn form a unique chemosensor and mechanoreceptor neuronal cell complex that releases highly-ordered secretion products upon stimulation. The phylum Cnidaria includes the corals, hydras, jellyfish, Portuguese men-of-war, sea anemones, sea pens, sea whips, and sea fans. Cnidaria are taxonomically subdivided into: Anthozoa (Hexacorallia and Octocorallia) with the absence of a medusa stage, and the Medusozoa, that usually exhibit a medusa stage in their life cycle and includes the classes Cubozoa, Hydrozoa, Scyphozoa, and Staurozoa [1] (Figure1). The Cnidaria are one of the earliest branches in the animal tree, with tissue layers, muscles, and sense organs. They are diploblastic, have a radial symmetry, do not possess a real brain having only two cell layers; the epithelial cells are involved in all the innate immune responses. The endodermal epithelium functions as a chemical barrier using antimicrobial peptides, while the ectodermal epithelium represents a physicochemical barrier. Furthermore, Cnidaria are present in the fossil record since the Precambrian, when the other animals similar to the present ones were absent [1,2]. Mar. Drugs 2018, 16, 296; doi:10.3390/md16090296 www.mdpi.com/journal/marinedrugs Mar. Drugs 2018, 16, 296 2 of 15 Mar. Drugs 2018, 16, x 2 of 15 Figure 1. The phylogenetic relationships of Medusozoa (Staurozoa, Hydrozoa, Cubozoa, and Scyphozoa) andFigure Anthozoa 1. The as reportedphylogenetic by Boero relationships et al. [1]. Molecular of Medusozoa data sustain (Staurozoa, the separation Hydrozoa, in two Cubozoa, class of theand Anthozoa,Scyphozoa) which and areAnthozoa common as distinguished reported by Boero by tentacles et al. [1]. morphology. Molecular Octocorallia data sustain is the a group separation of hard in coraltwo class species of the living Anthozoa, at a depth which of more are common than 100 distinguished m. This is a veryby tentacles slow growing morphology. species, Octocorallia formed by is polypsa group with of eighthard coral tentacles species which living capture at a floatingdepth of materials more than of up100 to m. several This is hundred a very slow microns growing and includedspecies, softformed corals. by Hexacoralliapolyps with iseight a group tentacles of several which hundred capture reef-building floating materials coral species of up includingto several stonyhundred coral microns and sea and anemones. included The soft polyps corals. of thisHexacorallia coral have is tentaclesa group inof groupsseveral ofhundred six, instead reef-building of eight. coral species including stony coral and sea anemones. The polyps of this coral have tentacles in Severalgroups of important six, instead issues of eight. related to immunity can be inferred from the diversity in cnidarian life histories and habitats. In particular, in some cases their life cycles are very long and they may Several important issues related to immunity can be inferred from the diversity in cnidarian life be subjected to repeated exposure to pathogenic agents [2]. Consequently, in the absence of specific histories and habitats. In particular, in some cases their life cycles are very long and they may be immune cells, cnidarians must have effective mechanisms to defend against microbial pathogens. subjected to repeated exposure to pathogenic agents [2]. Consequently, in the absence of specific Furthermore, colonial forms, in order to save tissue integrity, rely on their capacity of self/nonself immune cells, cnidarians must have effective mechanisms to defend against microbial pathogens. discrimination to rapidly recognize approaching allogeneic cells as foreign and to remove them [3]. Furthermore, colonial forms, in order to save tissue integrity, rely on their capacity of self/nonself Finally, successful growth for cnidarians is related to their capacity to differentiate between beneficial discrimination to rapidly recognize approaching allogeneic cells as foreign and to remove them [3]. symbionts and pathogenic intruders [4,5], since they are colonized by complex bacterial communities Finally, successful growth for cnidarians is related to their capacity to differentiate between and in several cases constitute home to algal symbionts. On account of these considerations it is of beneficial symbionts and pathogenic intruders [4,5], since they are colonized by complex bacterial interest to understand how animal’s longevity have modified the defense to innate components of communities and in several cases constitute home to algal symbionts. On account of these immunity, leading us to consider Cnidaria as good candidates at the crossroad of metazoan evolution. considerations it is of interest to understand how animal’s longevity have modified the defense to Several molecular “omics” studies on the hydrozoans [6,7] sea anemones [8,9] and corals [8,10,11] innate components of immunity, leading us to consider Cnidaria as good candidates at the crossroad demonstrated that some genes, associated with the immune responses, resulted conserved from of metazoan evolution. Several molecular “omics” studies on the hydrozoans [6,7] sea anemones cnidarians to vertebrates. [8,9] and corals [8,10,11] demonstrated that some genes, associated with the immune responses, 2.resulted Cnidarians conserved Associated from cnidarians Microbial Communitiesto vertebrates. 2. CnidariansMarine microorganisms Associated Microbial are present Communities at high density representing a major component in terms of the biomass on Earth. By the advent of the powerful tools of the molecular biology, remote sensing, and deepMarine sea microorganisms exploration, amazing are present discoveries at high on density the abundance representing and a diversity major component of marine in microbial terms of lifethe and biomass its function on Earth. in global By the ecology advent have of the been powerful made. tools In particular, of the molecular researches biology, on the relationshipsremote sensing, of microbialand deep componentssea exploration, with amazing other organisms discoveries have on furnished the abundance new information and diversity on of the marine phenomena microbial of foodlife and networks, its function symbiosis in global and pathogenicityecology have been [12,13 made.]. In particular, researches on the relationships of microbialRecently, components there has been with increasing other organisms interest have in microbesfurnished as new a relevant information portion on the of thephenomena animal phenotype,of food networks, responsible symbiosis for theand fitnesspathogenicity as well [12,13]. as the ecological features of their hosts [14,15]. SeveralRecently, studies accomplishedthere has been by increasing genetic and interest genomic in approachesmicrobes as have a relevant provided portion evidence of forthe severalanimal animal–bacteriaphenotype, responsible interactions for inthe invertebrates fitness as well and as vertebrates the ecological revealing features that of bacteriatheir hosts play [14,15]. a crucial Several role studies accomplished by genetic and genomic approaches have provided evidence for several animal–bacteria interactions in invertebrates and vertebrates revealing that bacteria play a crucial role in facilitating animals’ origin and evolution [16,17]. Moreover, these findings clarified that Mar. Drugs 2018, 16, 296 3 of 15 Mar. Drugs 2018, 16, x 3 of 15 animalsin facilitating
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