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631.
Hloïse Rouz Pierre E. Galand Mnica Medina Pim Bongaerts Michel Pichon Gonzalo Prez-Rosales Gergely Torda Aurelie Moya Under The Pole Consortium Jean-Baptiste Raina Laetitia Hdouin 《The ISME journal》2021,15(5):1564
The symbiosis between scleractinian corals and photosynthetic algae from the family Symbiodiniaceae underpins the health and productivity of tropical coral reef ecosystems. While this photosymbiotic association has been extensively studied in shallow waters (<30 m depth), we do not know how deeper corals, inhabiting large and vastly underexplored mesophotic coral ecosystems, modulate their symbiotic associations to grow in environments that receive less than 1% of surface irradiance. Here we report on the deepest photosymbiotic scleractinian corals collected to date (172 m depth), and use amplicon sequencing to identify the associated symbiotic communities. The corals, identified as Leptoseris hawaiiensis, were confirmed to host Symbiodiniaceae, predominantly of the genus Cladocopium, a single species of endolithic algae from the genus Ostreobium, and diverse communities of prokaryotes. Our results expand the reported depth range of photosynthetic scleractinian corals (0–172 m depth), and provide new insights on their symbiotic associations at the lower depth extremes of tropical coral reefs.Subject terms: Symbiosis, Microbial ecologyThe ecological success of scleractinian corals, the engineers of one of the most productive and diverse ecosystems on Earth, relies on a myriad of symbiotic associations with microorganisms [1]. Among these symbioses, the association between the coral host and unicellular algae from the family Symbiodiniaceae is central to coral health and powers the metabolically expensive process of calcification [2]. The coral host provides limited inorganic nutrients, while Symbiodiniaceae share essential organic compounds derived from their photosynthetic activity [3]. This light-dependent association has mainly been studied in shallow waters (<30 m) because of technical limitations imposed by traditional scientific scuba diving. However, photosynthetic scleractinian corals have been observed in the mesophotic reef slope down to 150–165 m depth [4, 5].As depth increases, the waveband of solar radiation used by most algae for photosynthesis (from 400–700 nm) becomes attenuated in both intensity and width. Even in clear tropical waters, the irradiance levels below 120 m depth can be less than 1% of surface values, and the light spectrum is shifted toward the blue and blue–green wavelengths (~475 nm) (e.g. [4]). These light limitations pose a major constraint for the productivity of benthic organisms that rely on photosynthetic symbionts [6], including reef-building corals (scleractinians). While the scleractinian coral species Leptoseris hawaiiensis has been reported to occur as deep as 153 m in Hawaii and 165 m at Johnston atoll (reviewed in [4]), no live specimens were collected at these extreme depths. The fact that Symbiodiniaceae have been found at much greater depth in association with Antipatharians (396 m) [7], raises the possibility that they might also be present in scleractinian corals deeper than 165 m. Previous studies have genetically confirmed and identified endosymbiotic Symbiodiniaceae in Leptoseris down to 70 m on the Great Barrier Reef [8] and down to 125 m depth in Hawaii [9–11]. A specific host-Symbiodiniaceae association was reported between deep L. hawaiiensis and a Cladocopium from the ancestral C1 radiation [9–11], which represents a diverse group of Symbiodiniaceae commonly found in association with scleractinians on shallow coral reefs [8, 9, 12, 13]. To better understand how scleractinian corals can survive so far away from their presumed light optimum, it is critical to determine if these deep specimens (1) maintain their association with photosynthetic algae and/or (2) if their survival in the deepest mesophotic coral ecosystems requires a shift in their microbial communities, including Symbiodiniaceae and other microorganisms such as endolithic algae and bacteria.Here we report on the observation and collection of the deepest scleractinian corals in association with Symbiodiniaceae and other photosymbionts. Technical divers using closed-circuit rebreathers recovered three L. hawaiiensis colonies from the Gambier archipelago (French Polynesia, Fig. 1A) at 154, 168, and 172 m depth (n = 2 subsamples for each depth; Fig. 1B–D). Irradiance measured at 120 m depth was <2% of that recorded at 6 m depth and irradiance at 172 m was predicted to be <1% (Fig.(Fig.1E1E and S1). ITS2 sequencing revealed Symbiodiniaceae presence in all three lower mesophotic colonies sampled, with nearly all of the retrieved amplicon sequence variants (ASVs; with most of these representing intragenomic sequence variants) classified as Cladocopium (Fig. 2). The most common ITS2 ASV representative sequence associated with these Leptoseris hosts (S-01, Fig. 2 and S2; 50–57% of total ASVs in each sample) was C1 (GeoSymbio and SymPortal databases; see supplementary methods). This represents one of the most common groups of Symbiodiniaceae, and it has previously been reported in Leptoseris [9, 10, 14], as well as other host species at depths ranging from the surface to 125 m [8, 10, 11, 13–15]. As a complementary approach, ITS2 profiles predicted by SymPortal were used as proxy for Symbiodiniaceae genotypes ([16]; see supplementary methods and data files S1–S4). These predicted ITS2 profiles were largely consistent among replicates but confirmed a different profile for the colony at 172 m depth compared to those at 154 and 168 m depth (Fig. S2). Nonetheless, the Symbiodiniaceae communities shared three ASVs that exactly matched C89 (S-02: 5% at 172 m vs. 17–19% at 154–168 m) and two different C variants (both S-05 and S-07: 7% at 172 m vs. ~2% at 154–168 m) in public databases (Fig. S3; GeoSymbio, SymPortal or Genbank). Of the 26 ASVs identified across all samples, one sequence originated from Durusdinium (S-24 D1 with GeoSymbio and SymPortal databases). This sequence is found in multiple heat-tolerant Durusdinium species including the enigmatic, cosmopolitan [17], host generalist D. trenchii [18]. However, whether or not the Symbiodiniaceae sampled here is D. trenchii or indeed thermally tolerant cannot be confirmed without further genetic and phenotypic data. Low abundance ASVs were observed at all three depths (172 m: 8 ASVs, 154 and 168 m: 10 ASVs, Fig. S3), including nine ASV sequences (Fig. 2) that have not been reported previously in the GeoSymbio [13] and SymPortal (access date: 2020-05-19_07-23-40) [16] databases (Fig. S3). Comparison of the overall Symbiodiniaceae SymPortal predicted ITS2 profiles (Fig. S2) did not confidently identify matches with previously encountered profiles (predominantly from shallow reef environments), indicating that they might be specific to this species and/or mesophotic environment. Given the extreme paucity of light at these depths, we hypothesize that lower mesophotic L. hawaiiensis may use different strategies to photoacclimate. Morphologically, the coral species were characterized by a thin flat skeleton (Fig. 1B–D), which is optimal for light harvesting and reducing skeletal carbonate deposition [19]. Leptoseris hawaiiensis has also been shown to display depth-associated physiological specialization and trophic plasticity (acquiring energy from different food sources) [9], and an unusual light-harvesting system, which enlarges the spectrum of wavelengths for photosynthesis by transforming the short, blue-shifted wavelength with their autofluorescent pigments [19].Open in a separate windowFig. 1Sampling location of the deepest photosymbiotic scleractinian coral recorded to date.A Map of the Gambier archipelago, French Polynesia. Pictures of Leptoseris hawaiiensis collected at 172 m depth in the Gambier archipelago (B) during the in situ sampling (screenshot of video © UTP III), (C) after reaching the surface and (D) after bleaching for taxonomic identification with the green color indicating the presence of endolithic algae. E Variation of the optical index of irradiance (in PAR) along the coral reef depth gradient from 6 to 120 m depth (predictions for 150 and 172 m depths) at Mangareva. For each depth, the three values represent a mean value for 3 days of measurements recorded every 5 min with a PAR logger (DEFI2-L Advantech) at three different time periods of the day (9 h30–10 h00, 12 h30–13 h00 and 15 h30–16 h00).Open in a separate windowFig. 2Microbial communities harbored by the three deep colonies.Composition of the microbial community in Leptoseris hawaiiensis collected at 172, 168, and 154 m. At each depth, two subsamples were analyzed for each colony. The ITS2 marker shows the relative proportion of different Symbiodiniaceae ASVs (with GeoSymbio and SymPortal v.2020-05-19_07-23-40 affiliations). The 16S rDNA marker shows the relative proportions of different ASVs for endolithic algae chloroplast composition and bacteria classes. Asterisk represents sequences with no exact match in the SymPortal database for Symbiodiniaceae.To identify other microorganisms associated with our lower mesophotic scleractinian colonies, we targeted the 16S rRNA gene (V4–V5 region; see supplementary methods). Sequencing data revealed the presence of green algal chloroplast sequences belonging to the genus Ostreobium (Fig. 2). This endolithic alga was abundant in the deep coral colonies as suggested by the marked green color observed below the living tissues (Fig. 1C) and within the skeleton after removing the soft tissues in bleach (Fig. 1D). We identified a single Ostreobium species (ASV ga-01), belonging to clade 2, that was dominant in all the colonies (Fig. 2 and S4), and has been previously reported across the depth gradient in scleractinian corals and octocorals worldwide [20, 21]. The nature of the interaction between corals and Ostreobium has been debated. Evidence supports a mutualistic association under extreme conditions such as coral stress (inducing bleaching) [22] or drastically reduced light exposure [23]. Under the low light conditions of the deep mesophotic fore reef slope, Ostreobium might complement Symbiodiniaceae’s function by providing photosynthates to the host. These endolithic algae are adapted to photosynthesize in near-darkness with increased numbers of light-harvesting xanthophyll pigments that can use shorter wavelengths compared to other green algae and optimize light capture (e.g. [24]).Bacteria associated with the lower mesophotic scleractinian colonies had an observed richness ranging from 106 to 211 ASVs per sample (Fig. S5). These bacteria mainly belonged to the classes Alpha- (19-49%) and Gamma-proteobacteria (8–17%), Bacteroidia (6–20%) and subgroup-6 of Acidobacteria (1–17%) (Fig. 2), which are known to associate with corals [25]. In total, we detected 843 different bacterial ASVs, among which 67–89% were unique to one colony or even unique to one subsample (Fig. S6 and Table S1). Our data suggest that the coral hosts displayed individual microbial signatures with some common ASVs shared between subsamples of the same colony (Fig. S6). However, this result might have been affected by the low-sequencing depth of the microbiome following the removal of the Ostreobium reads. Our results corroborate previous reports describing the high intra-specific variability of coral-associated bacterial communities at different spatial scales (e.g. [25, 26]), which might be driven by biological traits, such as the age [27] or diets of the colonies [28].This study reports a new depth record for scleractinian corals associated with symbiotic algae at 172 m. Similar to conspecifics previously sampled in mesophotic environments between 115 and 125 m depth [10], the deepest L. hawaiiensis reported here associated with symbiotic-microalgae belonging to the highly diverse C1 lineage. The deep colonies were also characterized by the presence and abundance of a single species of endolithic alga from the genus Ostreobium (clade 2). These filamentous green algae adapted to thrive in extreme low light conditions [24] might highly contribute to the survival of L. hawaiiensis at depth through photosynthates translocation [29]. In addition, bacterial communities were diverse, with intraspecific differences in community composition. Our findings provide new insights into the symbioses of scleractinian corals at depth, through the conservation of their associated photosymbiotic algae, raising important questions about the nature and mechanisms involved in the interactions between host and Symbiodiniaceae and/or Ostreobium (e.g. evolutionary theory of symbiosis [30]). Future studies should establish the contribution of photosynthetic symbionts to the energy budget of mesophotic corals. Understanding the biology of ecosystem engineers, such as tropical reef corals, living at the edge of their habitat range is important to determine the plasticity of these organisms and their ability to withstand environmental pressure. 相似文献
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633.
Florent Laferrière Philippe Tixador Mohammed Moudjou Jér?me Chapuis Pierre Sibille Laetitia Herzog Fabienne Reine Emilie Jaumain Hubert Laude Human Rezaei Vincent Béringue 《PLoS pathogens》2013,9(10)
Prions are proteinaceous infectious agents responsible for fatal neurodegenerative diseases in animals and humans. They are essentially composed of PrPSc, an aggregated, misfolded conformer of the ubiquitously expressed host-encoded prion protein (PrPC). Stable variations in PrPSc conformation are assumed to encode the phenotypically tangible prion strains diversity. However the direct contribution of PrPSc quaternary structure to the strain biological information remains mostly unknown. Applying a sedimentation velocity fractionation technique to a panel of ovine prion strains, classified as fast and slow according to their incubation time in ovine PrP transgenic mice, has previously led to the observation that the relationship between prion infectivity and PrPSc quaternary structure was not univocal. For the fast strains specifically, infectivity sedimented slowly and segregated from the bulk of proteinase-K resistant PrPSc. To carefully separate the respective contributions of size and density to this hydrodynamic behavior, we performed sedimentation at the equilibrium and varied the solubilization conditions. The density profile of prion infectivity and proteinase-K resistant PrPSc tended to overlap whatever the strain, fast or slow, leaving only size as the main responsible factor for the specific velocity properties of the fast strain most infectious component. We further show that this velocity-isolable population of discrete assemblies perfectly resists limited proteolysis and that its templating activity, as assessed by protein misfolding cyclic amplification outcompetes by several orders of magnitude that of the bulk of larger size PrPSc aggregates. Together, the tight correlation between small size, conversion efficiency and duration of disease establishes PrPSc quaternary structure as a determining factor of prion replication dynamics. For certain strains, a subset of PrP assemblies appears to be the best template for prion replication. This has important implications for fundamental studies on prions. 相似文献
634.
Laetitia Bonifait Marc Veillette Valérie Létourneau Daniel Grenier Caroline Duchaine 《Applied and environmental microbiology》2014,80(11):3296-3304
Streptococcus suis is an important swine pathogen that can cause septicemia, meningitis, and pneumonia. Also recognized as an emerging zoonotic agent, it is responsible for outbreaks of human infections in Asian countries. Serotype 2 is the predominant isolate from diseased animals and humans. The aerosolization of S. suis in the air of swine confinement buildings (SCB) was studied. The presence of S. suis in bioaerosols was monitored in SCB where cases of infection had been reported and in healthy SCB without reported infections. Using a quantitative-PCR (qPCR) method, we determined the total number of bacteria (1 × 108 to 2 × 108 airborne/m3), total number of S. suis bacteria (4 × 105 to 10 × 105 airborne/m3), and number of S. suis serotype 2 and 1/2 bacteria (1 × 103 to 30 × 103 airborne/m3) present in the air. S. suis serotypes 2 and 1/2 were detected in the air of all growing/finishing SCB that had documented cases of S. suis infection and in 50% of healthy SCB. The total number of bacteria and total numbers of S. suis and S. suis serotype 2 and 1/2 bacteria were monitored in one positive SCB during a 5-week period, and it was shown that the aerosolized S. suis serotypes 2 and 1/2 remain airborne for a prolonged period. When the effect of aerosolization on S. suis was observed, the percentage of intact S. suis bacteria (showing cell membrane integrity) in the air might have been up to 13%. Finally S. suis was found in nasal swabs from 14 out of 21 healthy finishing-SCB workers, suggesting significant exposure to the pathogen. This report provides a better understanding of the aerosolization, prevalence, and persistence of S. suis in SCB. 相似文献
635.
Laetitia G. E. Wilkins 《Molecular ecology》2019,28(21):4693-4696
Evolutionary adaptation is the adjustment of species to a new or changing environment. Engaging in mutualistic microbial symbioses has been put forward as a key trait that promotes the differential, evolutionary success of many animal and plant lineages (McFall‐Ngai, 2008). Microbial mutualists allow these organisms to occupy new ecological niches where they could not have persisted on their own or would have been constrained by competitors. Vertical transmission of beneficial microbial symbionts from parents to the offspring is expected to link the adaptive association between a given host and microbe, and it can lead to coevolution and sometimes even cospeciation (Fisher, Henry, Cornwallis, Kiers, & West, 2017). Vertical transmission also causes bottlenecks that strongly reduce the effective population size and genetic diversity of the symbiont population. Moreover, vertically transmitted symbionts are assumed to have fewer opportunities to exchange genes with relatives in the environment. In a “From the Cover” article in this issue of Molecular Ecology, Breusing, Johnson, Vrijenhoek, and Young (2019) investigated whether hybridization among different host species could lead to interspecies exchange of otherwise strictly vertically transmitted symbionts. Hybridization of divergent lineages can potentially cause intrinsic and extrinsic incompatibilities, swamp rare alleles, and lead to population extinctions. In some cases, however, it might also create novel trait combinations that lead to evolutionary innovation (Marques, Meier, & Seehausen, 2019). Breusing et al. (2019) linked the concept of hybridization to symbiont transmission, and their findings have significant implications for the study of evolution of vertically transmitted symbionts and their hosts. 相似文献
636.
637.
638.
639.
Paule Bénit Eric Letouzé Malgorzata Rak Laetitia Aubry Nelly Burnichon Judith Favier Anne-Paule Gimenez-Roqueplo Pierre Rustin 《BBA》2014
Seventy years from the formalization of the Krebs cycle as the central metabolic turntable sustaining the cell respiratory process, key functions of several of its intermediates, especially succinate and fumarate, have been recently uncovered. The presumably immutable organization of the cycle has been challenged by a number of observations, and the variable subcellular location of a number of its constitutive protein components is now well recognized, although yet unexplained. Nonetheless, the most striking observations have been made in the recent period while investigating human diseases, especially a set of specific cancers, revealing the crucial role of Krebs cycle intermediates as factors affecting genes methylation and thus cell remodeling. We review here the recent advances and persisting incognita about the role of Krebs cycle acids in diverse aspects of cellular life and human pathology. 相似文献
640.
Divorce and remating in birds can be described as strategies used to enhance reproductive success. Mate switching often occurs because pairs failed to brood at least one chick during the previous breeding season. In the present study, we evaluated the influence of reproductive success on female preferences in domesticated canaries (Serinus canaria). For that purpose, females previously paired and having reared young were placed in a choice test situation: They were allowed to choose between their previous mate and a familiar male (a male neighbor during the breeding period). During these choice tests, females tended to stay near their previous mate longer than near a male neighbor when their reproductive success was “good” (at least two chicks). On the other hand, females with “poor” reproductive success (one chick) did not show a preference for their previous mate. Furthermore, in the present study, we observed that during choice tests males reacted to the presence of their previous mate in a particular way, by gathering nest material. This behavior was more scarcely observed in neighbor males which, on the contrary, sang significantly more than previous mates did. 相似文献