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Presence of Lactic Acid Bacteria in the Intestinal Tract of the Mediterranean Trout (Salmo Macrostigma) in Its Natural Environment

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Presence of Lactic Acid Bacteria in the Intestinal Tract of the Mediterranean Trout (Salmo Macrostigma) in Its Natural Environment life Article Presence of Lactic Acid Bacteria in the Intestinal Tract of the Mediterranean Trout (Salmo macrostigma) in Its Natural Environment Massimo Iorizzo , Gianluca Albanese, Bruno Testa * , Mario Ianiro, Francesco Letizia, Mariantonietta Succi, Patrizio Tremonte, Mariasilvia D’Andrea , Nicolaia Iaffaldano and Raffaele Coppola Department of Agriculture, Environmental and Food Sciences, University of Molise, Via De Sanctis, 86100 Campobasso, Italy; [email protected] (M.I.); [email protected] (G.A.); [email protected] (M.I.); [email protected] (F.L.); [email protected] (M.S.); [email protected] (P.T.); [email protected] (M.D.); [email protected] (N.I.); [email protected] (R.C.) * Correspondence: [email protected] Abstract: Knowledge of the composition of the gut microbiota in freshwater fish living in their natural habitat has taxonomic and ecological importance. Few reports have been produced on the composition of the gut microbiota and on the presence of LAB in the intestines of freshwater fish that inhabit river environments. In this study, we investigated the LAB community that was present in the gastrointestinal tract (GIT) of Mediterranean trout (Salmo macrostigma) that colonized the Biferno and Volturno rivers of the Molise region (Italy). The partial 16S rRNA gene sequences of these strains were determined for the species-level taxonomic placement. The phylogenetic analysis revealed that the Citation: Iorizzo, M.; Albanese, G.; isolated LABs belonged to seven genera (Carnobacterium, Enterococcus, Lactobacillus, Lactiplantibacillus, Testa, B.; Ianiro, M.; Letizia, F.; Vagococcus, Lactococcus, and Weissella). The study of the enzymatic activities showed that these LABs Succi, M.; Tremonte, P.; D’Andrea, M.; could contribute to the breakdown of polysaccharides, proteins, and lipids. In future studies, a Iaffaldano, N.; Coppola, R. greater understanding of how the LABs act against pathogens and trigger the fish immune response Presence of Lactic Acid Bacteria in the may provide practical means to engineer the indigenous fish microbiome and enhance disease control Intestinal Tract of the Mediterranean and fish health. Trout (Salmo macrostigma) in Its Natural Environment. Life 2021, 11, Keywords: lactic acid bacteria; gut microbiota; Mediterranean trout; river environment 667. https://doi.org/10.3390/ life11070667 Academic Editor: Peter Deines 1. Introduction Received: 27 April 2021 The intestinal tracts of fishes contain a complex and dynamic community of microor- Accepted: 5 July 2021 ganisms [1,2]. Among them, the lactic acid bacteria (LAB) play an important role due to Published: 7 July 2021 some of their properties: production of antimicrobial substances and improved disease re- sistance, greater antioxidative stress tolerance, immune response stimulation, and increase Publisher’s Note: MDPI stays neutral in the availability of nutrients [3–5]. LABs were among the first living organisms on Earth; with regard to jurisdictional claims in they appeared about three billion years ago in the transition period from anaerobiosis to published maps and institutional affil- aerobiosis. They seem to have adapted well to both anaerobic and aerobic life conditions iations. since they bear all the necessary proteins for respiration and several enzymes involved in fermentative pathways [6]. Several species of LABs belonging to the Lactobacillus, Lacto- coccus, Leuconostoc, Enterococcus, Streptococcus, Carnobacterium, Pediococcus, and Weissella genera have adapted to grow under very different environmental conditions and are impor- Copyright: © 2021 by the authors. tant representatives of the gut microbiota of both freshwater and marine fish [7]. In recent Licensee MDPI, Basel, Switzerland. decades, numerous studies have shown that different intrinsic and extrinsic factors affect This article is an open access article the level, composition, and/or diversity of the fish gut microbiota: life stage, trophic level, distributed under the terms and diet, seasonality, habitat, stress, sex, and phylogeny [8–10]. LAB’s diversity was particularly conditions of the Creative Commons studied in freshwater fish, but few reports have been produced on the composition of the Attribution (CC BY) license (https:// gut microbiota and on the presence of LABs in the intestines of freshwater fish that inhabit creativecommons.org/licenses/by/ river environments [11–14]. 4.0/). Life 2021, 11, 667. https://doi.org/10.3390/life11070667 https://www.mdpi.com/journal/life Life 2021, 11, x FOR PEER REVIEW 2 of 14 reports have been produced on the composition of the gut microbiota and on the presence Life 2021, 11, 667 of LABs in the intestines of freshwater fish that inhabit river environments [11–14].2 of 13 Knowledge of the composition of the gut microbiota in freshwater fish living in their natural habitat has taxonomic and ecological importance. In particular, the study of the gut Knowledgemicrobiome of thein compositionthreatened ofwildlife the gut microbiotaspecies has in freshwaterenormous fish potential living in theirto improve naturalconservation habitat hasefforts taxonomic and to and gain ecological insights importance. into the In particular,host–microbe the study coevolution. of the The gut microbiome in threatened wildlife species has enormous potential to improve con- interaction of animals with their respective symbiotic microorganisms can provide servation efforts and to gain insights into the host–microbe coevolution. The interaction ofimportant animals with tools their for respective the management symbiotic microorganismsof various issues canprovide related important to the protection tools of forendangered the management animal ofspecies various [15]. issues Salmo related macrostigma to the protection is an endemic of endangered freshwater animal trout species speciesof the Mediterranean [15]. Salmo macrostigma area (Figureis an endemic 1). This freshwater salmonid trout is protected species of theby Mediterraneanthe Habitats Directive area92/43/EEC (Figure 1and). This is considered salmonid isa protected“vulnerable by thespec Habitatsies” in Europe Directive and 92/43/EEC “critically and endangered” is consideredin Italy [16]. a “vulnerable The diet species”of the Mediterranean in Europe and “critically trout consists endangered” mainly in of Italy macrozoobenthos, [16]. The dietlarvae of theand Mediterranean adult insects, trout and consists to a lesser mainly extent, of macrozoobenthos, vegetable elements, larvae andcrustaceans, adult and insects,mollusks. and Macroinvertebrates to a lesser extent, vegetable and fry elements, and small crustaceans, fish, as well and as mollusks. being food Macroin- competitors, vertebratesalso represent and a fry valid and source small fish,of nourishment as well as being in the food vital competitors, stages of the also Mediterranean represent a trout. valid source of nourishment in the vital stages of the Mediterranean trout. The water The water temperature in this species’ thermal niches is between 7 and 15 °C, which is the temperature in this species’ thermal niches is between 7 and 15 ◦C, which is the optimal survivaloptimal range survival for this range cold for stenothermal this cold fishstenothermal species [17– 20fish]. In species this study, [17–20]. we investigated In this study, we theinvestigated LAB community the LAB present community in the gastrointestinal present in tract the (GIT) gastrointestinal of the Mediterranean tract (GIT) trout of the (MediterraneanSalmo macrostigma trout) that (Salmo inhabits macrostigma river environments.) that inhabits At present river environments. no similar studies At are present no availablesimilar studies on this freshwaterare available fish on species. this freshwater fish species. FigureFigure 1. 1.Adult Adult specimen specimen of Mediterraneanof Mediterranean trout. trout. 2. Materials and Methods 2. Materials and Methods 2.1. Lactic Acid Bacteria (LAB) Isolation 2.1. Lactic Acid Bacteria (LAB) Isolation A total of 18 adult specimens of Mediterranean trout that accidentally died in the fish traps usedA total in the of scientific18 adult activitiesspecimens of the of LIFEMediterranean Nat. Sal. Mo trout Project that (LIFE17 accidentally NAT/IT/000547) died in the fish wastraps collected. used Thein the fish werescientific taken fromactivities 7 different of the study LIFE sites onNat. the BifernoSal. Mo (4 sites)Project and (LIFE17 VolturnoNAT/IT/000547) (3 sites) rivers was (Molisecollected. region, The Italy) fish betweenwere taken November from and7 different January study during sites the on the daily inspection of the fish traps and immediately transported in portable refrigerators Biferno◦ (4 sites) and Volturno (3 sites) rivers (Molise region, Italy) between November and (2–8JanuaryC) toduring the microbiology the daily laboratory.inspection Theof the exterior fish oftraps the fishand wasimmediately wiped clean transported with in 70% ethanol, the abdomen opened at the ventral midline, and the whole intestine was portable refrigerators (2–8 °C) to the microbiology laboratory. The exterior of the fish was aseptically removed from the abdominal cavity and separated into the proximal (pyloric ceca,wiped PC) clean and midgutwith 70% (MG) ethanol, sections the (Figure abdomen2). opened at the ventral midline, and the whole intestineOnce thewas specimens aseptically were removed longitudinally from opened,the abdominal the MG sections cavity wereand rinsedseparated using into the 3%proximal NaCl to (pyloric remove non-adherentceca,
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