scholarly journals Comparative Genomics Reveals Ecological and Evolutionary Insights into Sponge-Associated Thaumarchaeota

mSystems ◽  
2019 ◽  
Vol 4 (4) ◽  
Author(s):  
Shan Zhang ◽  
Weizhi Song ◽  
Bernd Wemheuer ◽  
Julie Reveillaud ◽  
Nicole Webster ◽  
...  

ABSTRACT Thaumarchaeota are frequently reported to associate with marine sponges (phylum Porifera); however, little is known about the features that distinguish them from their free-living thaumarchaeal counterparts. In this study, thaumarchaeal metagenome-assembled genomes (MAGs) were reconstructed from metagenomic data sets derived from the marine sponges Hexadella detritifera, Hexadella cf. detritifera, and Stylissa flabelliformis. Phylogenetic and taxonomic analyses revealed that the three thaumarchaeal MAGs represent two new species within the genus Nitrosopumilus and one novel genus, for which we propose the names “Candidatus UNitrosopumilus hexadellus,” “Candidatus UNitrosopumilus detritiferus,” and “Candidatus UCenporiarchaeum stylissum” (the U superscript indicates that the taxon is uncultured). Comparison of these genomes to data from the Sponge Earth Microbiome Project revealed that “Ca. UCenporiarchaeum stylissum” has been exclusively detected in sponges and can hence be classified as a specialist, while “Ca. UNitrosopumilus detritiferus” and “Ca. UNitrosopumilus hexadellus” are also detected outside the sponge holobiont and likely lead a generalist lifestyle. Comparison of the sponge-associated MAGs to genomes of free-living Thaumarchaeota revealed signatures that indicate functional features of a sponge-associated lifestyle, and these features were related to nutrient transport and metabolism, restriction-modification, defense mechanisms, and host interactions. Each species exhibited distinct functional traits, suggesting that they have reached different stages of evolutionary adaptation and/or occupy distinct ecological niches within their sponge hosts. Our study therefore offers new evolutionary and ecological insights into the symbiosis between sponges and their thaumarchaeal symbionts. IMPORTANCE Sponges represent ecologically important models to understand the evolution of symbiotic interactions of metazoans with microbial symbionts. Thaumarchaeota are commonly found in sponges, but their potential adaptations to a host-associated lifestyle are largely unknown. Here, we present three novel sponge-associated thaumarchaeal species and compare their genomic and predicted functional features with those of closely related free-living counterparts. We found different degrees of specialization of these thaumarchaeal species to the sponge environment that is reflected in their host distribution and their predicted molecular and metabolic properties. Our results indicate that Thaumarchaeota may have reached different stages of evolutionary adaptation in their symbiosis with sponges.

2013 ◽  
Vol 79 (20) ◽  
pp. 6407-6413 ◽  
Author(s):  
E. Lambrecht ◽  
J. Baré ◽  
I. Van Damme ◽  
W. Bert ◽  
K. Sabbe ◽  
...  

ABSTRACTFree-living protozoa play an important role in the ecology and epidemiology of human-pathogenic bacteria. In the present study, the interaction betweenYersinia enterocolitica, an important food-borne pathogen, and the free-living amoebaAcanthamoeba castellaniiwas studied. Several cocultivation assays were set up to assess the resistance ofY. enterocoliticatoA. castellaniipredation and the impact of environmental factors and bacterial strain-specific characteristics. Results showed that allY. enterocoliticastrains persist in association withA. castellaniifor at least 14 days, and associations withA. castellaniienhanced survival ofYersiniaunder nutrient-rich conditions at 25°C and under nutrient-poor conditions at 37°C. Amoebae cultivated in the supernatant of oneYersiniastrain showed temperature- and time-dependent permeabilization. Intraprotozoan survival ofY. enterocoliticadepended on nutrient availability and temperature, with up to 2.8 log CFU/ml bacteria displaying intracellular survival at 7°C for at least 4 days in nutrient-rich medium. Transmission electron microscopy was performed to locate theYersiniacells inside the amoebae. AsYersiniaandAcanthamoebashare similar ecological niches, this interaction identifies a role of free-living protozoa in the ecology and epidemiology ofY. enterocolitica.


2021 ◽  
Vol 8 ◽  
Author(s):  
Christopher J. Freeman ◽  
Cole G. Easson ◽  
Cara L. Fiore ◽  
Robert W. Thacker

Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.


2020 ◽  
Author(s):  
Dimple Davray ◽  
Dipti Deo ◽  
Ram Kulkarni

Species belonging to the family Lactobacillaceae are found in highly diverse environments and play an important role in fermented foods and probiotic products. Many of these species have been individually reported to harbour plasmids that encode important genes. In this study, we performed comparative genomic analysis of publicly available data for 512 plasmids from 282 strains represented by 51 species of this family and correlated the genomic features of plasmids with the ecological niches in which these species are found. Two-thirds of the species had at least one plasmid-harbouring strain. Plasmid abundance and GC content were significantly lower in vertebrate-adapted species as compared to nomadic and free-living species. Hierarchical clustering highlighted the distinct nature of plasmids from the nomadic and free-living species than those from the vertebrate-adapted species. EggNOG-assisted functional annotation revealed that genes associated with transposition, conjugation, DNA repair and recombination, exopolysaccharide production, metal ion transport, toxin–antitoxin system, and stress tolerance were significantly enriched on the plasmids of the nomadic and in some cases nomadic and free-living species. On the other hand, genes related to anaerobic metabolism, ABC transporters and the major facilitator superfamily were overrepresented on the plasmids of the vertebrate-adapted species. These genomic signatures correlate with the comparatively nutrient-depleted, stressful and dynamic environments of nomadic and free-living species and nutrient-rich and anaerobic environments of vertebrate-adapted species. Thus, these results indicate the contribution of the plasmids in the adaptation of lactobacilli to their respective habitats. This study also underlines the potential application of these plasmids in improving the technological and probiotic properties of lactic acid bacteria.


2015 ◽  
Vol 82 (4) ◽  
pp. 1274-1285 ◽  
Author(s):  
Maya Britstein ◽  
Giulia Devescovi ◽  
Kim M. Handley ◽  
Assaf Malik ◽  
Markus Haber ◽  
...  

ABSTRACTSponges harbor a remarkable diversity of microbial symbionts in which signal molecules can accumulate and enable cell-cell communication, such as quorum sensing (QS). Bacteria capable of QS were isolated from marine sponges; however, an extremely small fraction of the sponge microbiome is amenable to cultivation. We took advantage of community genome assembly and binning to investigate the uncultured majority of sponge symbionts. We identified a completeN-acyl-homoserine lactone (AHL)-QS system (designated TswIR) and seven partialluxIhomologues in the microbiome ofTheonella swinhoei. The TswIR system was novel and shown to be associated with an alphaproteobacterium of the orderRhodobacterales, here termedRhodobacteralesbacterium TS309. ThetswIgene, when expressed inEscherichia coli, produced three AHLs, two of which were also identified in aT. swinhoeisponge extract. The taxonomic affiliation of the 16S rRNA ofRhodobacteralesbacterium TS309 to a sponge-coral specific clade, its enrichment in sponge versus seawater and marine sediment samples, and the presence of sponge-specific features, such as ankyrin-like domains and tetratricopeptide repeats, indicate a likely symbiotic nature of this bacterium.


mSystems ◽  
2019 ◽  
Vol 4 (4) ◽  
Author(s):  
Ilia Burgsdorf ◽  
Kim M. Handley ◽  
Rinat Bar-Shalom ◽  
Patrick M. Erwin ◽  
Laura Steindler

ABSTRACT “Candidatus Synechococcus feldmannii” is a facultative intracellular symbiont of the Atlanto-Mediterranean sponge Petrosia ficiformis. Genomic information of sponge-associated cyanobacteria derives thus far from the obligate and extracellular symbiont “Candidatus Synechococcus spongiarum.” Here we utilized a differential methylation-based approach for bacterial DNA enrichment combined with metagenomics to obtain the first draft genomes of “Ca. Synechococcus feldmannii.” By comparative genomics, we revealed that some genomic features (e.g., iron transport mediated by siderophores, eukaryotic-like proteins, and defense mechanisms, like CRISPR-Cas [clustered regularly interspaced short palindromic repeats-associated proteins]) are unique to both symbiont types and absent or rare in the genomes of taxonomically related free-living cyanobacteria. These genomic features likely enable life under the conditions found inside the sponge host. Interestingly, there are many genomic features that are shared by “Ca. Synechococcus feldmannii” and free-living cyanobacteria, while they are absent in the obligate symbiont “Ca. Synechococcus spongiarum.” These include genes related to cell surface structures, genetic regulation, and responses to environmental stress, as well as the composition of photosynthetic genes and DNA metabolism. We speculate that the presence of these genes confers on “Ca. Synechococcus feldmannii” its facultative nature (i.e., the ability to respond to a less stable environment when free-living). Our comparative analysis revealed that distinct genomic features depend on the nature of the symbiotic interaction: facultative and intracellular versus obligate and extracellular. IMPORTANCE Given the evolutionary position of sponges as one of the earliest phyla to depart from the metazoan stem lineage, studies on their distinct and exceptionally diverse microbial communities should yield a better understanding of the origin of animal-bacterium interactions. While genomes of several extracellular sponge symbionts have been published, the intracellular symbionts have, so far, been elusive. Here we compare the genomes of two unicellular cyanobacterial sponge symbionts that share an ancestor but followed different evolutionary paths—one became intracellular and the other extracellular. Counterintuitively, the intracellular cyanobacteria are facultative, while the extracellular ones are obligate. By sequencing the genomes of the intracellular cyanobacteria and comparing them to the genomes of the extracellular symbionts and related free-living cyanobacteria, we show how three different cyanobacterial lifestyles are reflected by adaptive genomic features.


2018 ◽  
Vol 84 (8) ◽  
Author(s):  
Stefano Romano

ABSTRACTMembers of the genusPseudovibriohave been isolated worldwide from a great variety of marine sources as both free-living and host-associated bacteria. So far, the available data depict a group of alphaproteobacteria characterized by a versatile metabolism, which allows them to use a variety of substrates to meet their carbon, nitrogen, sulfur, and phosphorous requirements. Additionally,Pseudovibrio-related bacteria have been shown to proliferate under extreme oligotrophic conditions, tolerate high heavy-metal concentrations, and metabolize potentially toxic compounds. Considering this versatility, it is not surprising that they have been detected from temperate to tropical regions and are often the most abundant isolates obtained from marine invertebrates. Such an association is particularly recurrent with marine sponges and corals, animals that play a key role in benthic marine systems. The data so far available indicate that these bacteria are mainly beneficial to the host, and besides being involved in major nutrient cycles, they could provide the host with both vitamins/cofactors and protection from potential pathogens via the synthesis of antimicrobial secondary metabolites. In fact, the biosynthetic abilities ofPseudovibriospp. have been emerging in recent years, and both genomic and analytic studies have underlined how these organisms promise novel natural products of biotechnological value.


2018 ◽  
Vol 84 (17) ◽  
Author(s):  
Wei Yan ◽  
Shuzhen Wei ◽  
Qiong Wang ◽  
Xilin Xiao ◽  
Qinglu Zeng ◽  
...  

ABSTRACTProchlorococcusis the most abundant and smallest known free-living photosynthetic microorganism and is a key player in marine ecosystems and biogeochemical cycles.Prochlorococcuscan be broadly divided into high-light-adapted (HL) and low-light-adapted (LL) clades. In this study, we isolated two low-light-adapted clade I (LLI) strains from the western Pacific Ocean and obtained their genomic data. We reconstructedProchlorococcusevolution based on genome rearrangement. Our results showed that genome rearrangement might have played an important role inProchlorococcusevolution. We also found that theProchlorococcusclades with streamlined genomes maintained relatively high synteny throughout most of their genomes, and several regions served as rearrangement hotspots. Backbone analysis showed that different clades shared a conserved backbone but also had clade-specific regions, and the genes in these regions were associated with ecological adaptations.IMPORTANCEProchlorococcus, the most abundant and smallest known free-living photosynthetic microorganism, plays a key role in marine ecosystems and biogeochemical cycles.Prochlorococcusgenome evolution is a fundamental issue related to howProchlorococcusclades adapted to different ecological niches. Recent studies revealed that the gene gain and loss is crucial to the clade differentiation. The significance of our research is that we interpreted theProchlorococcusgenome evolution from the perspective of genome structure and associated the genome rearrangement with theProchlorococcusclade differentiation and subsequent ecological adaptation.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Kazutoshi Yoshitake ◽  
Gaku Kimura ◽  
Tomoko Sakami ◽  
Tsuyoshi Watanabe ◽  
Yukiko Taniuchi ◽  
...  

AbstractAlthough numerous metagenome, amplicon sequencing-based studies have been conducted to date to characterize marine microbial communities, relatively few have employed full metagenome shotgun sequencing to obtain a broader picture of the functional features of these marine microbial communities. Moreover, most of these studies only performed sporadic sampling, which is insufficient to understand an ecosystem comprehensively. In this study, we regularly conducted seawater sampling along the northeastern Pacific coast of Japan between March 2012 and May 2016. We collected 213 seawater samples and prepared size-based fractions to generate 454 subsets of samples for shotgun metagenome sequencing and analysis. We also determined the sequences of 16S rRNA (n = 111) and 18S rRNA (n = 47) gene amplicons from smaller sample subsets. We thereafter developed the Ocean Monitoring Database for time-series metagenomic data (http://marine-meta.healthscience.sci.waseda.ac.jp/omd/), which provides a three-dimensional bird’s-eye view of the data. This database includes results of digital DNA chip analysis, a novel method for estimating ocean characteristics such as water temperature from metagenomic data. Furthermore, we developed a novel classification method that includes more information about viruses than that acquired using BLAST. We further report the discovery of a large number of previously overlooked (TAG)n repeat sequences in the genomes of marine microbes. We predict that the availability of this time-series database will lead to major discoveries in marine microbiome research.


2021 ◽  
Vol 9 (1) ◽  
pp. 171
Author(s):  
Yitayal S. Anteneh ◽  
Qi Yang ◽  
Melissa H. Brown ◽  
Christopher M. M. Franco

The misuse and overuse of antibiotics have led to the emergence of multidrug-resistant microorganisms, which decreases the chance of treating those infected with existing antibiotics. This resistance calls for the search of new antimicrobials from prolific producers of novel natural products including marine sponges. Many of the novel active compounds reported from sponges have originated from their microbial symbionts. Therefore, this study aims to screen for bioactive metabolites from bacteria isolated from sponges. Twelve sponge samples were collected from South Australian marine environments and grown on seven isolation media under four incubation conditions; a total of 1234 bacterial isolates were obtained. Of these, 169 bacteria were tested in media optimized for production of antimicrobial metabolites and screened against eleven human pathogens. Seventy bacteria were found to be active against at least one test bacterial or fungal pathogen, while 37% of the tested bacteria showed activity against Staphylococcus aureus including methicillin-resistant strains and antifungal activity was produced by 21% the isolates. A potential novel active compound was purified possessing inhibitory activity against S. aureus. Using 16S rRNA, the strain was identified as Streptomyces sp. Our study highlights that the marine sponges of South Australia are a rich source of abundant and diverse bacteria producing metabolites with antimicrobial activities against human pathogenic bacteria and fungi.


mBio ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Radames J. B. Cordero ◽  
Emma Camacho ◽  
Arturo Casadevall

ABSTRACT The fungal human pathogen Cryptococcus neoformans undergoes melanization in response to nutrient starvation and exposure to exogenous melanin precursors. Melanization protects the fungus against host defense mechanisms such as oxidative damage and other environmental stressors (e.g., heat/cold stress, antimicrobial compounds, ionizing radiation). Conversely, the melanization process generates cytotoxic intermediates, and melanized cells are potentially susceptible to overheating and to certain melanin-binding drugs. Despite the importance of melanin in C. neoformans biology, the signaling mechanisms regulating its synthesis are poorly understood. The recent report by D. Lee, E.-H. Jang, M. Lee, S.-W. Kim, et al. [mBio 10(5):e02267-19, 2019, https://doi.org/10.1128/mBio.02267-19] provides new insights into how C. neoformans regulates melanization. The authors identified a core melanin regulatory network consisting of transcription factors and kinases required for melanization under low-nutrient conditions. The redundant and epistatic connections of this melanin-regulating network demonstrate that C. neoformans melanization is complex and carefully regulated at multiple levels. Such complex regulation reflects the multiple functions of melanin in C. neoformans biology.


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