Detecting signatures of a sponge‐associated lifestyle in bacterial genomes

Díez‐Vives, Cristina; Esteves, Ana I. S.; Costa, Rodrigo; Nielsen, Shaun; Thomas, Torsten

doi:10.1111/1758-2229.12655

Cited by 12 publications

(13 citation statements)

References 50 publications

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“…In agreement with a recent permutational analysis in which no signature CDSs could be unequivocally identified for host‐associated Aquimarina strains (Díez‐Vives et al ., ), ordination of both COG (Fig. ) and Pfam profiles in our study revealed no correlation between isolation source (FL vs. HA) and functional genome clustering among the 26 strains examined.…”

Section: Resultsmentioning

confidence: 99%

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

Silva

Blom

Keller‐Costa

et al. 2019

Environmental Microbiology

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Summary This study determines the natural product biosynthesis and full coding potential within the bacterial genus Aquimarina. Using comprehensive phylogenomics and functional genomics, we reveal that phylogeny instead of isolation source [host‐associated (HA) vs. free‐living (FL) habitats] primarily shape the inferred metabolism of Aquimarina species. These can be coherently organized into three major functional clusters, each presenting distinct natural product biosynthesis profiles suggesting that evolutionary trajectories strongly underpin their secondary metabolite repertoire and presumed bioactivities. Aquimarina spp. are highly versatile bacteria equipped to colonize HA and FL microniches, eventually displaying opportunistic behaviour, owing to their shared ability to produce multiple glycoside hydrolases from diverse families. We furthermore uncover previously underestimated, and highly complex secondary metabolism for the genus by detecting 928 biosynthetic gene clusters (BGCs) across all genomes, grouped in 439 BGC families, with polyketide synthases (PKSs), terpene synthases and non‐ribosomal peptide synthetases (NRPSs) ranking as the most frequent BGCs encoding drug‐like candidates. We demonstrate that the recently described cuniculene (trans‐AT PKS) BGC is conserved among, and specific to, the here delineated A. megaterium‐macrocephali‐atlantica phylogenomic clade. Our findings provide a timely and in‐depth perspective of an under‐explored yet emerging keystone taxon in the cycling of organic matter and secondary metabolite production in marine ecosystems.

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Section: Resultsmentioning

confidence: 99%

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

Silva

Blom

Keller‐Costa

et al. 2019

Environmental Microbiology

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“…To gain further insights into thaumarchaeal adaptation to a sponge-associated lifestyle, indicator analysis (50) was undertaken for the relative abundance of orthologous groups (OGs) of proteins. Comparison of OGs has been extensively used to investigate the evolution of organisms and their potential functional adaptation to the environment or particular lifestyles (9, 32). OGs from sponge-associated “ Ca .…”

Section: Resultsmentioning

confidence: 99%

“…Phylogenetic analyses have shown that sponge microbiota often contain members of the phyla Proteobacteria (mainly Gamma - and Alphaproteobacteria ), Actinobacteria , Firmicutes , Chloroflexi , Nitrospirae , Cyanobacteria , “ Candidatus Poribacteria,” and Thaumarchaeota (4–6). Studies analyzing isolate genomes or metagenome-assembled genomes (MAGs) from a few of these bacterial phyla have postulated several adaptive features of sponge-associated symbionts compared to their free-living relatives, including an enrichment of unique eukaryotic-like proteins (ELPs) and methyltransferases in the cyanobacterial “ Candidatus Synechococcus spongiarum” (7–9), an abundance of diverse phyH domain proteins in Poribacteria (10), an enrichment of CRISPR-Cas systems, ABC transporters, and restriction-modification systems in the alphaproteobacterial Rhodospirillaceae (11), and functions related to carbohydrate uptake, phage defense, and protein secretion in sulfur-oxidizing Gammaproteobacteria (12, 13). In contrast, other Proteobacteria such as the genera Aquimarina and Pseudovibrio have few or no obvious features that distinguish them from their free-living counterparts (9).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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.

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“…Anti-sigma antagonist (COG1366) and serine phosphatase RsbU, regulator of sigma subunit (COG2208), were among the 17 orthologous groups found present in all genomes of free-living cyanobacteria and lacking from “ Ca . Synechococcus spongiarum” (141). Interestingly, eight of these orthologous groups, including COG1366 and COG2208, were shared between “ Ca .…”

Section: Resultsmentioning

confidence: 99%

Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont

et al. 2019

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“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.

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Detecting signatures of a sponge‐associated lifestyle in bacterial genomes

Cited by 12 publications

References 50 publications

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

Comparative genomics reveals complex natural product biosynthesis capacities and carbon metabolism across host‐associated and free‐living Aquimarina (Bacteroidetes, Flavobacteriaceae) species

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

Life at Home and on the Roam: Genomic Adaptions Reflect the Dual Lifestyle of an Intracellular, Facultative Symbiont

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