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Phylogeny resolved, metabolism revealed: functional radiation within a widespread and divergent clade of sponge symbionts.

ABSTRACT: The symbiosis between bacteria and sponges has arguably the longest evolutionary history for any extant metazoan lineage, yet little is known about bacterial evolution or adaptation in this process. An example of often dominant and widespread bacterial symbionts of sponges is a clade of uncultured and uncharacterised Proteobacteria. Here we set out to characterise this group using metagenomics, in-depth phylogenetic analyses, metatranscriptomics, and fluorescence in situ hybridisation microscopy. We obtained five metagenome-assembled-genomes (MAGs) from different sponge species that, together with a previously published MAG (AqS2), comprise two families within a new gammaproteobacterial order that we named ^UTethybacterales. Members of this order share a heterotrophic lifestyle but vary in their predicted ability to use various carbon, nitrogen and sulfur sources, including taurine, spermidine and dimethylsulfoniopropionate. The deep branching of the ^UTethybacterales within the Gammaproteobacteria and their almost exclusive presence in sponges suggests they have entered a symbiosis with their host relatively early in evolutionary time and have subsequently functionally radiated. This is reflected in quite distinct lifestyles of various species of ^UTethybacterales, most notably their diverse morphologies, predicted substrate preferences, and localisation within the sponge tissue. This study provides new insight into the evolution of metazoan-bacteria symbiosis.

SUBMITTER: Taylor JA

PROVIDER: S-EPMC8027453 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundEnvironmental SSU rDNA surveys have significantly improved our understanding of microeukaryotic diversity. Many of the sequences acquired using this approach are closely related to lineages previously characterized at both morphological and molecular levels, making interpretation of these data relatively straightforward. Some sequences, by contrast, appear to be phylogenetic orphans and are sometimes inferred to represent "novel lineages" of unknown cellular identity. Consequently, interpretation of environmental DNA surveys of cellular diversity rely on an adequately comprehensive database of DNA sequences derived from identified species. Several major taxa of microeukaryotes, however, are still very poorly represented in these databases, and this is especially true for diverse groups of single-celled parasites, such as gregarine apicomplexans.Methodology/principal findingsThis study attempts to address this paucity of dna sequence data by characterizing four different gregarine species, isolated from the intestines of crustaceans, at both morphological and molecular levels: Thiriotia pugettiae sp. n. from the graceful kelp crab (Pugettia gracilis), Cephaloidophora cf. communis from two different species of barnacles (Balanus glandula and B. balanus), Heliospora cf. longissima from two different species of freshwater amphipods (Eulimnogammarus verrucosus and E. vittatus), and Heliospora caprellae comb. n. from a skeleton shrimp (Caprella alaskana). SSU rDNA sequences were acquired from isolates of these gregarine species and added to a global apicomplexan alignment containing all major groups of gregarines characterized so far. Molecular phylogenetic analyses of these data demonstrated that all of the gregarines collected from crustacean hosts formed a very strongly supported clade with 48 previously unidentified environmental DNA sequences.Conclusions/significanceThis expanded molecular phylogenetic context enabled us to establish a major clade of intestinal gregarine parasites and infer the cellular identities of several previously unidentified environmental SSU rDNA sequences, including several sequences that have formerly been discussed broadly in the literature as a suspected "novel" lineage of eukaryotes.

Project description:BACKGROUND: The origin and early radiation of archosaurs and closely related taxa (Archosauriformes) during the Triassic was a critical event in the evolutionary history of tetrapods. This radiation led to the dinosaur-dominated ecosystems of the Jurassic and Cretaceous, and the high present-day archosaur diversity that includes around 10,000 bird and crocodylian species. The timing and dynamics of this evolutionary radiation are currently obscured by the poorly constrained phylogenetic positions of several key early archosauriform taxa, including several species from the Middle Triassic of Argentina (Gracilisuchus stipanicicorum) and China (Turfanosuchus dabanensis, Yonghesuchus sangbiensis). These species act as unstable 'wildcards' in morphological phylogenetic analyses, reducing phylogenetic resolution. RESULTS: We present new anatomical data for the type specimens of G. stipanicicorum, T. dabanensis, and Y. sangbiensis, and carry out a new morphological phylogenetic analysis of early archosaur relationships. Our results indicate that these three previously enigmatic taxa form a well-supported clade of Middle Triassic archosaurs that we refer to as Gracilisuchidae. Gracilisuchidae is placed basally within Suchia, among the pseudosuchian (crocodile-line) archosaurs. The approximately contemporaneous and morphologically similar G. stipanicicorum and Y. sangbiensis may be sister taxa within Gracilisuchidae. CONCLUSIONS: Our results provide increased resolution of the previously poorly constrained relationships of early archosaurs, with increased levels of phylogenetic support for several key early pseudosuchian clades. Moreover, they falsify previous hypotheses suggesting that T. dabanensis and Y. sangbiensis are not members of the archosaur crown group. The recognition of Gracilisuchidae provides further support for a rapid phylogenetic diversification of crown archosaurs by the Middle Triassic. The disjunct distribution of the gracilisuchid clade in China and Argentina demonstrates that early archosaurs were distributed over much or all of Pangaea although they may have initially been relatively rare members of faunal assemblages.

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Phylogeny resolved, metabolism revealed: functional radiation within a widespread and divergent clade of sponge symbionts.

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