skip to main content


Title: Symbiosis, Selection, and Novelty: Freshwater Adaptation in the Unique Sponges of Lake Baikal
Abstract Freshwater sponges (Spongillida) are a unique lineage of demosponges that secondarily colonized lakes and rivers and are now found ubiquitously in these ecosystems. They developed specific adaptations to freshwater systems, including the ability to survive extreme thermal ranges, long-lasting dessication, anoxia, and resistance to a variety of pollutants. Although spongillids have colonized all freshwater systems, the family Lubomirskiidae is endemic to Lake Baikal and plays a range of key roles in this ecosystem. Our work compares the genomic content and microbiome of individuals of three species of the Lubomirskiidae, providing hypotheses for how molecular evolution has allowed them to adapt to their unique environments. We have sequenced deep (>92% of the metazoan “Benchmarking Universal Single-Copy Orthologs” [BUSCO] set) transcriptomes from three species of Lubomirskiidae and a draft genome resource for Lubomirskia baikalensis. We note Baikal sponges contain unicellular algal and bacterial symbionts, as well as the dinoflagellate Gyrodinium. We investigated molecular evolution, gene duplication, and novelty in freshwater sponges compared with marine lineages. Sixty one orthogroups have consilient evidence of positive selection. Transporters (e.g., zinc transporter-2), transcription factors (aristaless-related homeobox), and structural proteins (e.g. actin-3), alongside other genes, are under strong evolutionary pressure in freshwater, with duplication driving novelty across the Spongillida, but especially in the Lubomirskiidae. This addition to knowledge of freshwater sponge genetics provides a range of tools for understanding the molecular biology and, in the future, the ecology (e.g., colonization and migration patterns) of these key species.  more » « less
Award ID(s):
1744877
NSF-PAR ID:
10156263
Author(s) / Creator(s):
; ; ;
Date Published:
Journal Name:
Molecular Biology and Evolution
Volume:
36
Issue:
11
ISSN:
0737-4038
Page Range / eLocation ID:
2462 to 2480
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Rivers and lake systems in the southern cone of South America have been widely influenced by historical glaciations, carrying important implications for the evolution of aquatic organisms, including prompting transitions between marine and freshwater habitats and by triggering hybridization among incipient species via waterway connectivity and stream capture events. Silverside fishes (Odontesthes) in the region comprise a radiation of 19 marine and freshwater species that have been hypothesized on the basis of morphological or mitochondrial DNA data to have either transitioned repeatedly into continental waters from the sea or colonized marine habitats following freshwater diversification. New double digest restriction‐site associated DNA data presented here provide a robust framework to investigate the biogeographical history of and habitat transitions inOdontesthes. We show thatOdontesthessilversides originally diversified in the Pacific but independently colonized the Atlantic three times, producing three independent marine‐to‐freshwater transitions. Our results also indicate recent introgression of marine mitochondrial haplotypes into two freshwater clades, with more recurring instances of hybridization among Atlantic‐ versus Pacific‐slope species. In Pacific freshwater drainages, hybridization with a marine species appears to be geographically isolated and may be related to glaciation events. Substantial structural differences of estuarine gradients between these two geographical areas may have influenced the frequency, intensity and evolutionary effects of hybridization events.

     
    more » « less
  2. Abstract

    Unveiling the tempo and mode of animal evolution is necessary to understand the links between environmental changes and biological innovation. Although the earliest unambiguous metazoan fossils date to the late Ediacaran period, molecular clock estimates agree that the last common ancestor (LCA) of all extant animals emerged ~850 Ma, in the Tonian period, before the oldest evidence for widespread ocean oxygenation at ~635–560 Ma in the Ediacaran period. Metazoans are aerobic organisms, that is, they are dependent on oxygen to survive. In low‐oxygen conditions, most animals have an evolutionarily conserved pathway for maintaining oxygen homeostasis that triggers physiological changes in gene expression via the hypoxia‐inducible factor (HIFa). However, here we confirm the absence of the characteristic HIFa protein domain responsible for the oxygen sensing of HIFa in sponges and ctenophores, indicating the LCA of metazoans lacked the functional protein domain as well, and so could have maintained their transcription levels unaltered under the very low‐oxygen concentrations of their environments. Using Bayesian relaxed molecular clock dating, we inferred that the ancestral gene lineage responsible for HIFa arose in the Mesoproterozoic Era, ~1273 Ma (Credibility Interval 957–1621 Ma), consistent with the idea that important genetic machinery associated with animals evolved much earlier than the LCA of animals. Our data suggest at least two duplication events in the evolutionary history of HIFa, which generated three vertebrate paralogs, products of the two successive whole‐genome duplications that occurred in the vertebrate LCA. Overall, our results support the hypothesis of a pre‐Tonian emergence of metazoans under low‐oxygen conditions, and an increase in oxygen response elements during animal evolution.

     
    more » « less
  3. Nikel, Pablo Ivan (Ed.)
    ABSTRACT Cultured Myxococcota are predominantly aerobic soil inhabitants, characterized by their highly coordinated predation and cellular differentiation capacities. Little is currently known regarding yet-uncultured Myxococcota from anaerobic, nonsoil habitats. We analyzed genomes representing one novel order (o__JAFGXQ01) and one novel family (f__JAFGIB01) in the Myxococcota from an anoxic freshwater spring (Zodletone Spring) in Oklahoma, USA. Compared to their soil counterparts, anaerobic Myxococcota possess smaller genomes and a smaller number of genes encoding biosynthetic gene clusters (BGCs), peptidases, one- and two-component signal transduction systems, and transcriptional regulators. Detailed analysis of 13 distinct pathways/processes crucial to predation and cellular differentiation revealed severely curtailed machineries, with the notable absence of homologs for key transcription factors (e.g., FruA and MrpC), outer membrane exchange receptor (TraA), and the majority of sporulation-specific and A-motility-specific genes. Further, machine learning approaches based on a set of 634 genes informative of social lifestyle predicted a nonsocial behavior for Zodletone Myxococcota . Metabolically, Zodletone Myxococcota genomes lacked aerobic respiratory capacities but carried genes suggestive of fermentation, dissimilatory nitrite reduction, and dissimilatory sulfate-reduction (in f_JAFGIB01) for energy acquisition. We propose that predation and cellular differentiation represent a niche adaptation strategy that evolved circa 500 million years ago (Mya) in response to the rise of soil as a distinct habitat on Earth. IMPORTANCE The phylum Myxococcota is a phylogenetically coherent bacterial lineage that exhibits unique social traits. Cultured Myxococcota are predominantly aerobic soil-dwelling microorganisms that are capable of predation and fruiting body formation. However, multiple yet-uncultured lineages within the Myxococcota have been encountered in a wide range of nonsoil, predominantly anaerobic habitats, and the metabolic capabilities, physiological preferences, and capacity of social behavior of such lineages remain unclear. Here, we analyzed genomes recovered from a metagenomic analysis of an anoxic freshwater spring in Oklahoma, USA, that represent novel, yet-uncultured, orders and families in the Myxococcota . The genomes appear to lack the characteristic hallmarks for social behavior encountered in Myxococcota genomes and displayed a significantly smaller genome size and a smaller number of genes encoding biosynthetic gene clusters, peptidases, signal transduction systems, and transcriptional regulators. Such perceived lack of social capacity was confirmed through detailed comparative genomic analysis of 13 pathways associated with Myxococcota social behavior, as well as the implementation of machine learning approaches to predict social behavior based on genome composition. Metabolically, these novel Myxococcota are predicted to be strict anaerobes, utilizing fermentation, nitrate reduction, and dissimilarity sulfate reduction for energy acquisition. Our results highlight the broad patterns of metabolic diversity within the yet-uncultured Myxococcota and suggest that the evolution of predation and fruiting body formation in the Myxococcota has occurred in response to soil formation as a distinct habitat on Earth. 
    more » « less
  4. Abstract Coral reefs are complex marine habitats that have been hypothesized to facilitate functional specialization and increased rates of functional and morphological evolution. Wrasses (Labridae: Percomorpha) in particular, have diversified extensively in these coral reef environments and have evolved adaptations to further exploit reef-specific resources. Prior studies have found that reef-dwelling wrasses exhibit higher rates of functional evolution, leading to higher functional variation than in non-reef dwelling wrasses. Here, we examine this hypothesis in the lower pharyngeal tooth plate of 134 species of reef and non-reef-associated labrid fishes using high-resolution morphological data in the form of micro-computed tomography scans and employing three-dimensional geometric morphometrics to quantify shape differences. We find that reef-dwelling wrasses do not differ from non-reef-associated wrasses in morphological disparity or rates of shape evolution. However, we find that some reef-associated species (e.g., parrotfishes and tubelips) exhibit elevated rates of pharyngeal jaw shape evolution and have colonized unique regions of morphospace. These results suggest that while coral reef association may provide the opportunity for specialization and morphological diversification, species must still be able to capitalize on the ecological opportunities to invade novel niche space, and that these novel invasions may prompt rapid rates of morphological evolution in the associated traits that allow them to capitalize on new resources. 
    more » « less
  5. Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships. 
    more » « less