Marine cyanobacteria in the anthropocene: Are top-down paradigms robust to climate change?

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: Top-down Vs Bottom-up Control and The Importance Of Scalementioning

confidence: 99%

Predation, community asynchrony, and metacommunity stability in cyanobacterial mats

2022

Preprint

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“…[x/y]/y), which would be useful for further analyzing the relationship between viral ecology and host abundance in this system. Taken together, these results highlight 1) the dire need to incorporate patterns from diverse contemporaneously unexplored microbial systems into theory and quantitative frameworks linking describing viral influence on microbial communities, and 2) the need to understand how biotic and abiotic context can drive fine-scale nuance in virus-microbe trophic interactions and contribute to patterns that depart from, and overwhelmingly subvert, general predictions from theory (53).…”

Section: Discussionmentioning

confidence: 88%

“…Our data overall suggest that viruses exert considerable influence over the dynamics of mat building populations and likely are major players in modulating the functional ecology of cyanobacterial mats on reefs. Viruses should be increasingly considered when exploring patterns in the demography and ecophysiology of cyanobacterial mats toward holistically understanding the causes and consequences of mat proliferation on coral reefs (53).…”

Section: Discussionmentioning

confidence: 99%

“…Viral impact on microbial mat systems, including coral reef cyanobacterial mats, is not yet readily predictable without system-specific characterization (51,52). The directionality of trophic interactions among viruses and their hosts may experience fine-scale dynamism dependent on density, host physiological state, and host trophic membership (27,53), and thus may not be generalizable across time. Furthermore, living as a biofilm is generally known to confer some protection from viral predation (54), especially in spatially structured (generally biologically mediated) biofilm communities (25).…”

Section: Introductionmentioning

confidence: 99%

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Top-heavy trophic structure within benthic viral dark matter

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.

“…The net effects are likely to display strong taxon‐ and context‐dependent relationships, similar to the effects synthesized in a recent meta‐analysis between coral disease incidence and predator presence for the family Scaridae (Renzi et al, 2022), which may be unequally driven by differences in environmental context or feeding mode (Nicolet et al, 2018). Furthermore, we hypothesized that strong context dependence may emerge between different complex biotic and abiotic axes, driving variability in the consumption of cyanobacterial mats (Cissell & McCoy, 2022), and differential contributions from unique mat morphotypes to total foraging. The systematic assessment of vectoring capabilities through in situ and ex situ experimentation is needed to understand the trade‐offs between the top‐down control of mat abundance versus mats as secondary vectors.…”

Section: Five Priority Research Areasmentioning

confidence: 99%

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

Eckrich²,

Ecological Applications

2022

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The concurrent rise in the prevalence of conspicuous benthic cyanobacterial mats and the incidence of coral diseases independently mark major axes of degradation of coral reefs globally. Recent advances have uncovered the potential for the existence of interactions between the expanding cover of cyanobacterial mats and coral disease, especially black band disease (BBD), and this intersection represents both an urgent conservation concern and a critical challenge for future research. Here, we propose links between the transmission of BBD and benthic cyanobacterial mats. We provide molecular and ecophysiological evidence suggesting that cyanobacterial mats may create and maintain physically favorable benthic refugia for BBD pathogens while directly harboring BBD precursor assemblages, and discuss how mats may serve as direct (mediated via contact) and indirect (mediated via predator-prey-pathogen relationships) vectors for BBD pathogens. Finally, we identify and outline future priority research directions that are aligned with actionable management practices and priorities to support evidence-based coral conservation practices.