Cyanobacterial mats as benthic reservoirs and vectors for coral black band disease pathogens

2022

Preprint

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Holistically characterizing mechanisms that connect biotic context with patterns in persistence across levels of ecological organization requires integrating patterns of variability across scale. This is especially true in microbial communities, where relevant trophic interactions operate across disparate spatiotemporal scales. Here, we integrated observational, experimental, and theoretical approaches to unify local and regional ecological processes driving the dynamics of benthic cyanobacterial mats on coral reefs off the island of Bonaire, Caribbean Netherlands. Community and metacommunity dynamics of mats were tracked for 49 days alongside quantification of macropredation pressure from fishes. Viral interactions were interrogated using shotgun metagenomics and metatranscriptomics within a dying mat community to explore patterns in viral infectivity and prey population dynamics. Further, we employed a field experiment to test the hypothesis that enhanced predation would result in decreased mat persistence. Finally, we constructed a cellular automaton model to predict patterns in mat metacommunity dynamics across different scenarios of top-down and bottom-up control and dispersal. Cyanobacterial mat metacommunities were temporally stable across the study, stabilized by asynchrony in the dynamics of communities (~54% death rate in communities across 10 death dates). A total of 11 different reef fishes were documented foraging on mats, exhibiting heterogeneity in predation pressure among communities (72.8 mean bites per mat (+-) 111.2 bites SD) that likely contributes to the stabilizing asynchrony of community dynamics. Predation from reef fishes, though, may interact with other factors to influence mat community dynamics, as experimentally enhanced predation decreased the instantaneous mortality rate of mat communities over natural mat communities (-0.012 vs. -0.023). Viral linkage strength increased in decaying mat area over healthy mat area (median log abundance 2.41 vs. 2.27) alongside decreases in prey population abundances. Theoretical simulations suggested that dispersal conveys a rescuing effect on mat metacommunity abundance under scenarios of strong trophic control, and dispersal is likely an important but unexplored driver of observed benthic cyanobacterial mat dynamics. We contextualize our experimental work with a collection of curated natural history observations and a unifying definition of benthic cyanobacterial mats. These data establish critical baselines and generate hypotheses relevant to the processes maintaining cyanobacterial dominance of reefs.

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Predation, community asynchrony, and metacommunity stability in cyanobacterial mats

Cissell

2022

Preprint

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“…Cyanobacterial mats are taxonomically and functionally complex communities (38) that can dramatically alter reef nitrogen budgets via nitrogen fixation (39–41), and reef carbon budgets via fixation of inorganic carbon and subsequent release of dissolved organic carbon (42). These shifts in reef carbon chemistry can alter systemic microbial energetic budgets, and favor the proliferation and stability of pathogenic taxa (43), potentially including pathogenic taxa involved in coral disease (44). Horizontally-spreading reef cyanobacterial mat carpets are subject to dynamic predation pressure from generalist reef fishes and specialist invertebrate mesograzers (45, 46), with substantial geographic and morphotypic-dependence in predation risk from macro- and mesopredators (32, 47, 48).…”

Section: Introductionmentioning

confidence: 99%

Top-heavy trophic structure within benthic viral dark matter

Cissell

2022

Preprint

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Viruses exert considerable influence on microbial population dynamics and community structure, with cascading effects on ecosystem-scale biogeochemical cycling and functional trajectories. Creating broadly generalizable theory on viral trophic ecology requires further inquiry into historically unexplored microbial systems that currently lack empirically demonstrated patterns in viral infectivity, such as structurally complex benthic communities. This becomes increasingly relevant considering recently proposed revisions to the fundamental mechanisms that modulate the strength and direction viral trophic linkages. Here, we employed deep longitudinal multiomic sequencing to characterize the viral assemblage (including ssDNA, dsDNA, and dsRNA viruses) and profile lineage-specific host-virus interactions within benthic cyanobacterial mats sampled from Bonaire, Caribbean Netherlands, over a complete diel time-series, and reconstruct patterns in intra-mat trophic structure. We recovered 11,020 unique viral populations spanning at least 10 viral families across the orders Caudovirales, Petitvirales, and Mindivirales, with evidence for extensive genomic novelty from reference and environmental viral sequences. Analysis of coverage ratios of viral sequences and computationally predicted hosts spanning 15 phyla and 21 classes revealed virus:host abundance and activity ratios consistently exceeding 1:1, with overall power-law scaling indicating an increasingly top-heavy intra-mat trophic structure with significant top-down pressure. Diel activity of cyanophages showed clear temporal patterns that seem to follow host physiological condition. These data generate important hypotheses concerning taxon-dependent variation in the relative contribution of top-down vs. bottom-up forcing in driving mat community dynamics, and establish a useful database of viral sequences from this previously unexplored system toward the generation of generalizable trans-system theory on viral trophic ecology.

“…Overgrowth of corals causes significant tissue damage and reduces growth rates (Titlyanov et al 2007). BCMs may also act as reservoirs for potentially pathogenic bacteria (Cissell et al 2022), and the increased cover of BCMs has been correlated with an increase in coral disease (Reverter et al 2020). Additionally, benthic cyanobacteria inhibit coral larval recruitment and reduce their likelihood of survival (Kuffner et al 2006; Ritson-Williams et al 2020).…”

Section: Introductionmentioning

confidence: 99%

Preferential consumption of benthic cyanobacterial mats by Caribbean parrotfishes

Manning

2022

Preprint

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Cyanobacteria are ubiquitous on coral reefs and perform important ecosystem functions. Benthic cyanobacterial mats (BCMs) have become increasingly abundant on degraded reefs. While epilithic and endolithic benthic cyanobacteria are the primary trophic resource for many parrotfishes, mat-forming benthic cyanobacteria are generally considered unpalatable to reef fishes. Regardless, recent studies have documented substantial grazing of BCMs by reef fishes, including parrotfishes. Here, we observed foraging in five Caribbean parrotfishes on the fringing coral reefs of Bonaire, Netherlands, to investigate BCM consumption relative to other benthic substrates. All species overwhelmingly targeted reef substrates composed of algal turfs and crustose coralline algae, which are typically associated with epilithic and endolithic microalgal and cyanobacterial communities. Additionally, three species preferentially consumed BCMs. As such, our work is consistent with and provides direct evidence supporting the recently proposed trophic role for parrotfishes as microphages. Contrasting observations of reef fishes avoiding substrates dominated by BCMs on other reefs suggests variation in the palatability of BCMs to grazing reef fishes, or species-specific differences in preference for these potentially nutritional trophic resources.