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- Chemical diplomacy in male tilapia: urinary signal increases sex hormone and decreases aggressionPublication . Saraiva, João; Keller-Costa, Tina; Hubbard, Peter; Rato, Ana; Canario, AdelinoAndrogens, namely 11-ketotestosterone (11KT), have a central role in male fish reproductive physiology and are thought to be involved in both aggression and social signalling. Aggressive encounters occur frequently in social species, and fights may cause energy depletion, injury and loss of social status. Signalling for social dominance and fighting ability in an agonistic context can minimize these costs. Here, we test the hypothesis of a 'chemical diplomacy' mechanism through urinary signals that avoids aggression and evokes an androgen response in receiver males of Mozambique tilapia (Oreochromis mossambicus). We show a decoupling between aggression and the androgen response; males fighting their mirror image experience an unresolved interaction and a severe drop in urinary 11KT. However, if concurrently exposed to dominant male urine, aggression drops but urinary 11KT levels remain high. Furthermore, 11KT increases in males exposed to dominant male urine in the absence of a visual stimulus. The use of a urinary signal to lower aggression may be an adaptive mechanism to resolve disputes and avoid the costs of fighting. As dominance is linked to nest building and mating with females, the 11KT response of subordinate males suggests chemical eavesdropping, possibly in preparation for parasitic fertilizations.
- Metagenome-assembled genome sequences of three uncultured planktomarina sp. strains from the Northeast Atlantic OceanPublication . Marques, Matilde; Borges, Nuno; Silva, Sandra Godinho; da Rocha, Ulisses Nunes; Lago-Lestón, Asunción; Keller-Costa, Tina; Da Silva Costa, RodrigoWe report three metagenome-assembled genomes (MAGs) of Planktomarina strains from coastal seawater (Portugal) to help illuminate the functions of understudied Rhodobacteraceae bacteria in marine environments. The MAGs encode proteins involved in aerobic anoxygenic photosynthesis and a versatile carbohydrate metabolism, strengthening the role of Planktomarina species in oceanic carbon cycling.
- Genomic insights into aquimarina sp. strain EL33, a bacterial symbiont of the gorgonian coral eunicella labiata.Publication . Keller-Costa, Tina; Silva, Rúben; Lago-Lestón, Asunción; Costa, RodrigoTo address the metabolic potential of symbiotic Aquimarina spp., we report here the genome sequence of Aquimarina sp. strain EL33, a bacterium isolated from the gorgonian coral Eunicella labiata This first-described (to our knowledge) animal-associated Aquimarina genome possesses a sophisticated repertoire of genes involved in drug/antibiotic resistance and biosynthesis.
- Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable AlphaproteobacteriaPublication . Karimi, Elham; Keller-Costa, Tina; Slaby, Beate M; Cox, Cymon; da Rocha, Ulisses N; Hentschel, Ute; da Silva Costa, RodrigoMarine sponges are early-branching, filter-feeding metazoans that usually host complex microbiomes comprised of several, currently uncultivatable symbiotic lineages. Here, we use a low-carbon based strategy to cultivate low-abundance bacteria from Spongia officinalis. This approach favoured the growth of Alphaproteobacteria strains in the genera Anderseniella, Erythrobacter, Labrenzia, Loktanella, Ruegeria, Sphingorhabdus, Tateyamaria and Pseudovibrio, besides two likely new genera in the Rhodobacteraceae family. Mapping of complete genomes against the metagenomes of S. officinalis, seawater, and sediments confirmed the rare status of all the above-mentioned lineages in the marine realm. Remarkably, this community of low-abundance Alphaproteobacteria possesses several genomic attributes common to dominant, presently uncultivatable sponge symbionts, potentially contributing to host fitness through detoxification mechanisms (e.g. heavy metal and metabolic waste removal, degradation of aromatic compounds), provision of essential vitamins (e.g. B6 and B12 biosynthesis), nutritional exchange (especially regarding the processing of organic sulphur and nitrogen) and chemical defence (e.g. polyketide and terpenoid biosynthesis). None of the studied taxa displayed signs of genome reduction, indicative of obligate mutualism. Instead, versatile nutrient metabolisms along with motility, chemotaxis, and tight-adherence capacities - also known to confer environmental hardiness - were inferred, underlying dual host-associated and free-living life strategies adopted by these diverse sponge-associated Alphaproteobacteria.
- A multi-component pheromone in the urine of dominant male tilapia (Oreochromis mossambicus) reduces aggression in rivalsPublication . Keller-Costa, Tina; Saraiva, João L.; Hubbard, Peter; Barata, Eduardo Nuno; Canário, Adelino V. M.Males often use scent to communicate their dominance, and to mediate aggressive and breeding behaviors. In teleost fish, however, the chemical composition of male pheromones is poorly understood. Male Mozambique tilapia, Oreochromis mossambicus, use urine that signals social status and primes females to spawn. The urinary sex pheromone directed at females consists of 5 beta-pregnane-3 alpha,17 alpha,20 beta-triol 3-glucuronate and its 20 alpha-epimer. The concentration of these is positively correlated with male social rank. This study tested whether dominant male urine reduces aggression in receiver males, and whether the pregnanetriol 3-glucuronates also reduce male-male aggression. Males were allowed to fight their mirror image when exposed to either: i) water control or a chemical stimulus; ii) dominant male urine (DMU); iii) C18-solid phase (C18-SPE) DMU eluate; iv) C18-SPE DMU eluate plus filtrate; v) the two pregnanetriol 3-glucuronates (P3Gs); or vi) P3Gs plus DMU filtrate. Control males mounted an increasingly aggressive fight against their image over time. However, DMU significantly reduced this aggressive response. The two urinary P3Gs did not replicate the effect of whole DMU. Neither did the C18-SPE DMU eluate, containing the P3Gs, alone, nor the C18-SPE DMU filtrate to which the two P3Gs were added. Only exposure to reconstituted DMU (C18-SPE eluate plus filtrate) restored the aggression-reducing effect of whole DMU. Olfactory activity was present in the eluate and the polar filtrate in electro-olfactogram studies. We conclude that P3Gs alone have no reducing effect on aggression and that the urinary signal driving off male competition is likely to be a multi-component pheromone, with components present in both the polar and non-polar urine fractions.
- Muscular hypertrophy of urinary bladders in dominant tilapia facilitates the control of aggression through urinary signalsPublication . Keller-Costa, Tina; Lopes, O. S.; Almeida, O. G.; Hubbard, Peter; Iacovella, A.; Lima, M.; Barata, E. N.; Canario, Adelino V. M.The urination pattern of the Mozambique tilapia (Oreochromis mossambicus) depends on social context, and the olfactory potency of urine released depends on social rank (males) and reproductive status (females). This strongly suggests that urine mediates chemical communication in this species. The current study tested, firstly, whether urine production rate depends on sex or social status and, secondly, whether differences in urination pattern and volume of urine stored are associated with variation in the morphology of the urinary bladder. Finally, the effect of urination during aggressive male–male interactions was assessed. Urine production in catheterized fish depended neither on sex nor social status (males). Nevertheless, males had larger kidneys than females. Dominant males had heavier urinary bladders than subordinate males or females, mainly due to enlarged muscle fibres, thicker urothelium and a thicker smooth muscle layer. In male pairs wherein urination was prevented by temporary constriction of the genital papillae, social interaction escalated to aggression (mouth-to-mouth fighting) more rapidly and frequently than control pairs. This was accompanied by elevated plasma testosterone and 11-ketotestosterone levels. In control encounters, the male that initiated the aggressive behaviour was usually the winner of the subsequent fight; this did not happen when the males could not urinate. These results suggest that the larger, more muscular bladder of dominant males is an adaptation, facilitating higher urination frequency, post-renal modulation and storage of larger urine volumes for longer. It is likely that urinary pheromones modulate aggression in male–male encounters by providing information on the social rank and/or motivation of the emitter; males are unlikely to invest in costly highly aggressive fights if they judge their opponent to be more dominant. Thus, a morphological explanation for the differing urination patterns of dominant and subordinant males, and females, has been provided, and a possible function for this behaviour in male–male interactions is suggested.
- The freshwater Sponge Ephydatia Fluviatilis harbours diverse pseudomonas species (Gammaproteobacteria, Pseudomonadales) with broad-spectrum antimicrobial activityPublication . Keller-Costa, Tina; Jousset, Alexandre; van Overbeek, Leo; van Elsas, Jan Dirk; Costa, RodrigoBacteria are believed to play an important role in the fitness and biochemistry of sponges (Porifera). Pseudomonas species (Gammaproteobacteria, Pseudomonadales) are capable of colonizing a broad range of eukaryotic hosts, but knowledge of their diversity and function in freshwater invertebrates is rudimentary. We assessed the diversity, structure and antimicrobial activities of Pseudomonas spp. in the freshwater sponge Ephydatia fluviatilis. Polymerase Chain Reaction - Denaturing Gradient Gel Electrophoresis (PCR-DGGE) fingerprints of the global regulator gene gacA revealed distinct structures between sponge-associated and free-living Pseudomonas communities, unveiling previously unsuspected diversity of these assemblages in freshwater. Community structures varied across E. fluviatilis specimens, yet specific gacA phylotypes could be detected by PCR-DGGE in almost all sponge individuals sampled over two consecutive years. By means of whole-genome fingerprinting, 39 distinct genotypes were found within 90 fluorescent Pseudomonas isolates retrieved from E. fluviatilis. High frequency of in vitro antibacterial (49%), antiprotozoan (35%) and anti-oomycetal (32%) activities was found among these isolates, contrasting less-pronounced basidiomycetal (17%) and ascomycetal (8%) antagonism. Culture extracts of highly predation-resistant isolates rapidly caused complete immobility or lysis of cells of the protozoan Colpoda steinii. Isolates tentatively identified as P. jessenii, P. protegens and P. oryzihabitans showed conspicuous inhibitory traits and correspondence with dominant sponge-associated phylotypes registered by cultivation-independent analysis. Our findings suggest that E. fluviatilis hosts both transient and persistent Pseudomonas symbionts displaying antimicrobial activities of potential ecological and biotechnological value.
- Draft genome sequence of vibrio jasicida 20LP, an opportunistic bacterium isolated from fish larvaePublication . Sanches-Fernandes, Gracinda M. M.; Califano, Gianmaria; Keller-Costa, Tina; Castanho, Sara; Soares, Florbela; Ribeiro, Laura; Pousão-Ferreira, Pedro; Mata, Leonardo; Costa, RodrigoWe present the genome sequence of Vibrio jasicida 20LP, a bacterial strain retrieved from larvae of gilthead seabream (Sparus aurata), a highly valuable, model fish species in land-based aquaculture. Annotation of the V. jasicida 20LP genome reveals multiple genomic features potentially underpinning opportunistic associations with diverse marine animals.
- Chemical communication in tilapia: a comparison of Oreochromis mossambicus with O. niloticusPublication . Hubbard, Peter; Mota, Vasco; Keller-Costa, Tina; Silva, José P. da; Canario, Adelino V. M.In allopatric speciation species differentiation generally results from different selective pressures in different environments, and identifying the traits responsible helps to understand the isolation mechanism(s) involved. Male Mozambique tilapia (Oreochromis mossambicus) use urine to signal dominance; furthermore, 5-pregnane-3,17,20-triol-3-glucuronide (and its -epimer, 5-pregnane-3,17,20-triol-3-glucuronide), in their urine is a potent pheromone, the concentration of which is correlated with social status. The Nile tilapia (O. niloticus) is a close relative; species divergence probably resulted from geographical separation around 6 million years ago. This raises the question of whether the two species use similar urinary chemical cues during reproduction. The olfactory potency of urine, and crude extracts, from either species was assessed by the electro-olfactogram and the presence of the steroid glucuronides in urine from the Nile tilapia by liquid-chromatography/mass spectrometry. Both species showed similar olfactory sensitivity to urine and respective extracts from either species, and similar sensitivity to the steroid glucuronides. 5-pregnan-3,17,20-triol-3-glucuronide was present at high concentrations (approaching 0.5 mM) in urine from Nile tilapia, with 5-pregnan-3,17,20-triol-3-glucuronide present at lower concentrations, similar to the Mozambique tilapia. Both species also had similar olfactory sensitivity to estradiol-3-glucuronide, a putative urinary cue from females. Together, these results support the idea that reproductive chemical cues have not been subjected to differing selective pressure. Whether these chemical cues have the same physiological and behavioural roles in O. niloticus as O. mossambicus remains to be investigated.
- Olfactory sensitivity to steroid glucuronates in Mozambique tilapia suggests two distinct and specific receptors for pheromone detectionPublication . Keller-Costa, Tina; Canario, Adelino V. M.; Hubbard, PeterCichlids offer an exciting opportunity to understand vertebrate speciation; chemical communication could be one of the drivers of African cichlid radiation. Chemical signals mediate key aspects in the lives of vertebrates and often are species specific. Dominant male Mozambique tilapia [Oreochromis mossambicus (Peters 1852)] release a sex pheromone, 5 beta-pregnan-3 alpha,17 alpha,20 beta-triol 3-glucuronate and its 20 alpha-epimer, via their urine. The objective of this study was to assess the sensitivity, specificity and versatility of the olfactory system of O. mossambicus to other steroids and their conjugates using the electro-olfactogram. Oreochromis mossambicus was sensitive to several 3-glucuronidated steroids, but did not respond to prostaglandins, unconjugated steroids or 17- or 20-conjugated steroids. Stimulation of the olfactory epithelium with increasing concentrations (1 pmol l(-1) to 10 mu mol l(-1)) of 5 beta-pregnan-3 alpha, 17 alpha,20 beta-triol 3-glucuronate, 5 beta-pregnan-3 alpha, 17 alpha,20 beta-triol 3-glucuronate, 3 alpha,17 alpha-dihydroxy-5 beta-pregnan-20-one 3-glucuronate, etiocholanolone 3 alpha-glucuronate and 17 beta-estradiol 3-glucuronate produced characteristic sigmoidal concentration-response curves. However, tilapia were most sensitive to 17 beta-estradiol-3-glucuronate, which also had the lowest apparent EC50 and maximal response amplitude. Cross-adaptation and binary mixture experiments suggested that 5 beta,3 alpha-reduced pregnan-and androstan-3-glucuronates share (a) common olfactory receptor(s), whereas 17 beta-estradiol 3-glucuronate is detected via (a) distinct olfactory receptor(s). In conclusion, the Mozambique tilapia has evolved high olfactory sensitivity and specificity to 3-glucuronidated steroids through two distinct olfactory receptor types; one detecting a male sex pheromone and a second detecting 17 beta-estradiol 3-glucuronate, a putative female-derived signal. However, O. mossambicus differs markedly in its olfactory perception from the more recently derived East African cichlid Astatotilapia burtoni, suggesting that chemical communication could, indeed, be involved in speciation.