Microbial Community multi-omic analysis of marsh sediment post crustacean shell compost enrichment: pathogen emergence and community response

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This study used metagenomics and metatranscriptomics to show that adding crustacean shell compost to marsh sediment rapidly shifted microbial metabolism towards chitin degradation and sporulation, decreased key biogeochemical processes, and enriched for putative pathogens and virulence genes, including aerolysin.

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Abstract

Changes in nutrient availability can rapidly alter microbial processes in natural environments, with implications in biogeochemical cycling and pathogen emergence. Short-term, functional responses of microbial communities to nutrient amendment in coastal communities remain poorly understood, particularly in temperate environments. A 48-hour microcosm pulse experiment was completed in which paired metagenomic and metatranscriptomic sequencing were employed to examine how the decomposition of chitin rich substrates, namely crab and lobster shell compost, alters salt marsh microbiome structure and function. Within 48 hours of amendment, pronounced shifts in community metabolism were observed, including increased chitin degradation and utilization, stress-response, and sporulation. These responses coincided with marked decreases in genes associated with key biogeochemical processes, including carbon fixation, sulfur oxidation and reduction, and other metabolic pathways. Shell compost addition also enriched putative pathogens and virulence-associated genes, accompanied by modest transcriptional activation, notably aerolysin A (aerA) , which encodes the pore-forming exotoxin aerolysin. These results demonstrate temperate salt marsh sediment microbiomes can undergo shifts in community composition and function that is associated with chitin-rich nutrient perturbation. The sensitivity of temperate coastal systems to organic matter input and the potential for ecological and public-health relevant outcomes are underscored, notably given that chitin is among the most abundant and readily available bionutrients in aquatic ecosystems globally.
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Abstract Changes in nutrient availability can rapidly alter microbial processes in natural environments, with implications in biogeochemical cycling and pathogen emergence. Short-term, functional responses of microbial communities to nutrient amendment in coastal communities remain poorly understood, particularly in temperate environments. A 48-hour microcosm pulse experiment was completed in which paired metagenomic and metatranscriptomic sequencing were employed to examine how the decomposition of chitin rich substrates, namely crab and lobster shell compost, alters salt marsh microbiome structure and function. Within 48 hours of amendment, pronounced shifts in community metabolism were observed, including increased chitin degradation and utilization, stress-response, and sporulation. These responses coincided with marked decreases in genes associated with key biogeochemical processes, including carbon fixation, sulfur oxidation and reduction, and other metabolic pathways. Shell compost addition also enriched putative pathogens and virulence-associated genes, accompanied by modest transcriptional activation, notably aerolysin A (aerA), which encodes the pore-forming exotoxin aerolysin. These results demonstrate temperate salt marsh sediment microbiomes can undergo shifts in community composition and function that is associated with chitin-rich nutrient perturbation. The sensitivity of temperate coastal systems to organic matter input and the potential for ecological and public-health relevant outcomes are underscored, notably given that chitin is among the most abundant and readily available bionutrients in aquatic ecosystems globally. Competing Interest Statement CEY and LE are employees of New England Biolabs Inc., a manufacturer of restriction enzymes and molecular reagents. RRC and KDB have no conflicting interests to declare.

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