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.

Analyses of the genome and transcriptomes of endemic Baikal sponges (Lubomirskiidae)

“…Our results showed that the genome size of Lubomirskia baikalensis (as determined using GenomeScope) is between 558 and 565 million base pairs (Kenny et al, 2019). This is larger than almost all known marine sponge genomes.…”

Freshwater sponge hosts and their green algae symbionts: a tractable model to understand intracellular symbiosis

“…Several features of freshwater sponge biology make them excellent systems for studying the molecular and cellular pathways required for successful symbiosis yet freshwater sponge symbioses are poorly represented in the modern algal-based symbiosis literature. The emergence of molecular tools offers renewed opportunities to study sponge-based symbiotic systems, and freshwater sponges offer many tractable qualities of a model system to study intracellular symbioses (Kenny et al, 2019;Kenny et al, 2020).…”

“…Thus, freshwater sponges have the potential to shed light on symbiosis as well as a variety of important physiological features. Recent work by Kenny et al, (2019) has already shown that freshwater sponges have extensive gene duplications driving evolutionary novelty and have benefited from symbioses that allow them to live in challenging conditions. Given that E. muelleri has a higher gene content than most animals, nearly twice that of humans (Kenny et al, 2020), it may not be surprising to find a large number of taxonomic specific genes among those that are differentially expressed.…”

“…Furthermore, while GSTs are best known for their role as detoxification enzymes, they are known to carry out a variety of other functions including peroxidase and isomerase activities, inhibition of Jun N-terminal kinase, binding to a range of ligands, and several novel classes of non-mammalian GSTs have functions that are not related to oxidative stress. Given the extensive gene duplication in freshwater sponges that has been described (see Kenny et al, 2019;Kenny et al, 2020)…”

Peer Review #2 of "Freshwater sponge hosts and their green algae symbionts: a tractable model to understand intracellular symbiosis (v0.1)"

“…Much of the initial work centered on the ecological importance of photosynthetic sponges in freshwater ecosystems (e.g., Williamson, 1977;Williamson, 1979;Frost & Williamson, 1980) yet freshwater sponge symbioses are poorly represented in the modern algal-based symbiosis literature. The emergence of powerful molecular tools, however, offers renewed opportunities to study sponge-based symbiotic systems, which is aided by the fact that freshwater sponges offer many tractable qualities of a model system (Kenny et al, 2019;Kenny et al, 2020). With modern molecular and cellular tools, however, freshwater sponges are proving to be an exciting tool to study intracellular symbiosis.…”