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Biology subjects

Canfield, D. E.

Publications and source records attributed to Canfield, D. E..

8 recordsLinked to original sources

Decoding Demosponge Diversity: Bayesian Analysis of Biodiversity, Extinction Events and Environmental Influences throughout the Phanerozoic

Sponges (phylum Porifera) have been essential to marine ecosystems for over 600 million years, contributing to nutrient cycling, reef building, and ecological stability. Despite their evolutionary importance, the drivers of their diversity dynamics remain poorly understood. This study investigates the diversification patterns of Demospongiae, the largest class of sponges with a well-documented fossil record throughout the Phanerozoic Eon (541-0 Ma). Using fossil occurrence data and a Bayesian framework, we modeled origination and extinction rates to understand their evolutionary history. Our findings reveal key extinction events, including three previously unrecognized events in the Cambrian, Late Silurian, and Late Jurassic, alongside known events such as the Permian-Triassic and Triassic-Jurassic extinctions. Notably, there was no statistical evidence for mass extinction during the Late Ordovician or Late Devonian. Additionally, Demosponges underwent a significant decline prior to the Cretaceous-Paleogene extinction. To explore abiotic influences, we applied the Multivariate Birth-Death (MBD) model across all extinction events. This analysis identified correlations between major speciation and extinction events and key variables, including temperature, continental fragmentation, oxygen levels, and sea level, as well as geochemical proxies such as sulfur and strontium, which may reflect underlying drivers like anoxia, weathering, or tectonic activity. Temperature and oxygen levels, in particular, correlated with speciation and extinction during the Permian-Triassic extinction. These findings underscore the role of environmental fluctuations in shaping demosponge diversity and highlight the complex interplay between changes in abiotic factors and sponge evolution. Our work provides critical insights into the factors driving sponge biodiversity and offers perspectives on how modern sponges might respond to ongoing climate change. Significance StatementSponges are ancient and ecologically pivotal marine organisms that have persisted through Earths major environmental upheavals. Despite their resilience, the mechanisms driving their evolutionary responses to past climate shifts remain unclear. By leveraging the fossil record of Demospongiae, this study identifies previously unrecognized extinction events and elucidates how abiotic factors, including temperature and oxygen levels, shaped their diversity during these crises. These findings enhance our understanding of sponge evolutionary dynamics and resilience, offering critical insights into the vulnerability of marine ecosystems under current and future climate change scenarios.

paleontology↗

Oxygen production via NO dismutation in different ammonia oxidizers.

Ammonia oxidizing archaea (AOA) are widespread and highly abundant in nature. Despite their typical aerobic metabolism, they can be abundant in ecosystems where oxygen is scarce. Recent observations revealed that the AOA isolate Nitrosopumilus maritimus produces oxygen and dinitrogen at nanomolar concentrations, upon oxygen depletion through nitric oxide (NO) dismutation. Here, we explore NO dismutation capability in other ammonia oxidizers with different phylogenetic affinities and from different environmental settings. The organisms explored include three marine AOA, one soil AOA and two soil ammonia-oxidizing bacteria (AOB). Upon oxygen depletion all isolates accumulated oxygen. In incubations with 15N tracers with ongoing oxygen accumulation, the AOA strains Nitrosopumilus adriaticus and Nitrosopumilus viennensis produced 46N2O from nitrite. Transient 46N2O accumulation followed by 30N2 production was detected in the AOA strains Nitrosopumilus piranensis and Nitrosopumilus sp. CCS1, supporting the earlier observation that NO-dismutation is a common metabolism in AOA, albeit with physiological variations between different strains. An important physiological variable is the capability to reduce N2O to N2. The finding of oxygen production in several AOA, as well as AOB, indicates that this process is widely distributed among the tree of life and adds an explanation for their abundance in oxygen-depleted environments.

microbiology↗

Transcriptomic responses of sponge holobionts to in situ, seasonal anoxia and hypoxia

Deoxygenation can be fatal for many marine animals; however, some sponge species are tolerant of hypoxia and anoxia. Indeed, two sponge species, Eurypon sp. 2 and Hymeraphia stellifera, survive seasonal anoxia for months at a time. To understand their tolerance mechanisms, we performed differential gene expression analyses on the sponges, their mitochondria and their microbial symbionts under in situ conditions of normoxia, hypoxia and anoxia. Each species possessed a unique microbiome, but the microbiomes of each species were dominated by a species-specific Thaumarchaeon and a Gammaproteobacterium. Holobiont gene expression was species-and oxygen-level dependent, though there were some shared interspecific responses to deoxygenation. In general, few changes occurred in the expression of sponge metabolic genes as a function of oxygenation level, indicating that they may remain metabolically active under anoxia. However, ATP synthesis genes were significantly upregulated under hypoxia when compared to normoxia, and genes for DNA replication were downregulated. Mitochondrial gene expression was effectively unchanged under both hypoxia and anoxia. Nevertheless, both anoxia and hypoxia caused upregulation of heat shock proteins (HSPs), indicating cellular level adaptations to deoxygenation stress. A meta-analysis demonstrated that sponge transcriptional responses to anoxia were distinct from those displayed by other invertebrates while dormant, and the hypothesis of sponge dormancy under anoxia was not supported. Thaumarchaeota symbionts also upregulated stress response genes in hypoxia, while maintaining expression of oxygen-dependent metabolic pathways under hypoxia and anoxia. Gammaproteobacteria symbionts showed relatively few noteworthy changes in gene expression in response to anoxia but decreased metabolic gene expression in hypoxia. There was no clear evidence of upregulated anaerobic respiration in the transcriptomes of the sponge holobionts under anoxia or hypoxia. The tolerance of some sponges to prolonged anoxia warrants further investigation and could give them an advantage in future oceans following climate change as well as in ancient oceans when oxygen concentrations were lower than at present.

ecology↗

Metagenomic data for Halichondria panicea from Illumina and Nanopore sequencing and preliminary genome assemblies for the sponge and two microbial symbionts.

ObjectivesThese data were collected to generate a novel reference metagenome for the sponge Halichondria panicea and its microbiome for subsequent differential expression analyses. Data descriptionThese data include raw sequences from four separate sequencing runs of the metagenome of a single individual of Halichondria panicea - one Illumina MiSeq (2x300 bp, paired-end) run and three Oxford Nanopore Technologies (ONT) long-read sequencing runs, generating 53.8 and 7.42 Gbp respectively. Comparing assemblies of Illumina, ONT and an Illumina-ONT hybrid revealed the hybrid to be the best assembly, comprising 163 Mbp in 63,555 scaffolds (N50: 3,084). This assembly, however, was still highly fragmented and only contained 52% of core metazoan genes (with 77.9% partial genes), so it was also not complete. However, this sponge is an emerging model species for field and laboratory work, and there is considerable interest in genomic sequencing of this species. Although the resultant assemblies from the data presented here are suboptimal, this data note can inform future studies by providing an estimated genome size and coverage requirements for future sequencing, sharing additional data to potentially improve other suboptimal assemblies of this species, and outlining potential limitations and pitfalls of the combined Illumina and ONT approach to novel genome sequencing.

genomics↗

Oxygen production by an ammonia-oxidizing archaeon

Ammonia-oxidizing archaea (AOA) are one of the most abundant groups of microbes in the worlds oceans and are key players in the nitrogen cycle. Their energy metabolism, the oxidation of ammonia to nitrite, requires oxygen. Nevertheless, AOA are abundant in environments where oxygen is undetectable. In incubation experiments, where oxygen concentrations were resolved to the nanomolar range, we show that Nitrosopumilus maritimus produces oxygen (O2) and dinitrogen (N2). The pathway is not completely resolved, but it has nitric oxide as a key intermediate. Part of the oxygen produced is directly used for ammonia oxidation, while some accumulates in the surrounding environment. N. maritimus joins a small handful of organisms known to produce oxygen in the dark, and based on this ability, we re-evaluate their role in oxygen-depleted marine environments.

microbiology↗

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semi-enclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, though some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance. ImportanceThe oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated compared to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin, and that animal evolution was not limited by low-oxygen conditions.

microbiology↗

The global explosion of eukaryotic algae: the potential role of phosphorus?

There arose one of the most important ecological transitions in Earths history approximately 750 million years ago during the middle Neoproterozoic Era (1000 to 541 million years ago, Ma). Biomarker evidence suggests that around this time there was a rapid shift from a predominantly bacterial-dominated world to more complex ecosystems governed by eukaryotic primary productivity. The resulting Rise of the algae led to dramatically altered food webs that were much more efficient in terms of nutrient and energy transfer. Yet, what triggered this ecological shift? In this study we examined the theory that it was the alleviation of phosphorus (P) deficiency that gave eukaryotic alga the prime opportunity to flourish. We performed laboratory experiments on the cyanobacterium Synochystis salina and the eukaryotic algae Tetraselmis suecia and examined their ability to compete for phosphorus. Both these organisms co-occur in modern European coastal waters and are not known to have any allelopathic capabilities. The strains were cultured in mono and mixed cultures in chemostats across a range of dissolved organic phosphorus (DIP) conditions to reflect modern and ancient oceanic conditions of 0.2 M P and 2 M P, respectively. Our results show that the cyanobacteria outcompete the algae at the low input (0.2 M P) treatment, yet the eukaryotic algae were not completely excluded and remained a constant background component in the mixed-culture experiments. Also, despite its relatively large cell size, the algae T. suecia had a high affinity for DIP. With DIP input concentrations resembling modern-day levels (2 M), the eukaryotic algae could effectively compete against the cyanobacteria in terms of total biomass production. These results suggest that the availability of phosphorus could have influenced the global expansion of eukaryotic algae. However, P limitation does not seem to explain the complete absence of eukaryotic algae in the biomarker record before ca. 750 Ma.

ecology↗

Very few sites can reshape a phylogenetic tree

The history of animal evolution, and the relative placement of extant animal phyla in this history is, in principle, testable from phylogenies derived from molecular sequence data. Though datasets have increased in size and quality in the past years, the contribution of individual genes (and ultimately amino acid sites) to the final phylogeny is unequal across genes. Here we demonstrate that by removing a small fraction of sites that strongly favor one topology, it is possible produce a highly-supported tree of an alternate topology. We explore this approach using a dataset for animal phylogeny, and create a highly-supported tree with a monophyletic group of sponges and ctenophores, a topology not usually recovered. As nearly all gene sets are neither standardized nor representative of the entire genome, we conclude that there are only two possible ways to remedy this problem. One solution would need to use a fixed set of genes, which though not representative, is at least standardized. The other would be to construct phylogenies using all genes, thus limiting analysis to species with sequenced genomes.

evolutionary biology↗