Mechanistic strategies of microbial communities regulating lignocellulose deconstruction in a UK salt marsh

Daniel R Leadbeater,Anna M Alessi,Juliana Sanchez Alponti,Joe D Taylor,Yi Li,Neil C Bruce,Simon J Mcqueen-Mason,Adam A Dowle,Joseph P Bennett,Alexander T Setchfield,Nicola C Oates,Thorunn Helgason

doi:10.1186/s40168-020-00964-0

Abstract

BackgroundSalt marshes are major natural repositories of sequestered organic carbon with high burial rates of organic matter, produced by highly productive native flora. Accumulated carbon predominantly exists as lignocellulose which is metabolised by communities of functionally diverse microbes. However, the organisms that orchestrate this process and the enzymatic mechanisms employed that regulate the accumulation, composition and permanence of this carbon stock are not yet known. We applied meta-exo-proteome proteomics and 16S rRNA gene profiling to study lignocellulose decomposition in situ within the surface level sediments of a natural established UK salt marsh.ResultsOur studies revealed a community dominated by Gammaproteobacteria, Bacteroidetes and Deltaproteobacteria that drive lignocellulose degradation in the salt marsh. We identify 42 families of lignocellulolytic bacteria of which the most active secretors of carbohydrate-active enzymes were observed to be Prolixibacteracea, Flavobacteriaceae, Cellvibrionaceae, Saccharospirillaceae, Alteromonadaceae, Vibrionaceae and Cytophagaceae. These families secreted lignocellulose-active glycoside hydrolase (GH) family enzymes GH3, GH5, GH6, GH9, GH10, GH11, GH13 and GH43 that were associated with degrading Spartina biomass. While fungi were present, we did not detect a lignocellulolytic contribution from fungi which are major contributors to terrestrial lignocellulose deconstruction. Oxidative enzymes such as laccases, peroxidases and lytic polysaccharide monooxygenases that are important for lignocellulose degradation in the terrestrial environment were present but not abundant, while a notable abundance of putative esterases (such as carbohydrate esterase family 1) associated with decoupling lignin from polysaccharides in lignocellulose was observed.ConclusionsHere, we identify a diverse cohort of previously undefined bacteria that drive lignocellulose degradation in the surface sediments of the salt marsh environment and describe the enzymatic mechanisms they employ to facilitate this process. Our results increase the understanding of the microbial and molecular mechanisms that underpin carbon sequestration from lignocellulose within salt marsh surface sediments in situ and provide insights into the potential enzymatic mechanisms regulating the enrichment of polyphenolics in salt marsh sediments.2Bi9cdUnFhfykPyYYU2FLjVideo

Highlights

Salt marshes are highly productive intertidal ecosystems that generate an abundance of organic carbon in the form of lignocellulose, where net aerial primary productivity often exceeds 1–2 kg C m−2 year−1 [1,2,3]
Here, we identify a diverse cohort of previously undefined bacteria that drive lignocellulose degradation in the surface sediments of the salt marsh environment and describe the enzymatic mechanisms they employ to facilitate this process
Functional assignment of the meta-exo-proteome To identify the lignocellulolytic enzymes involved in biomass breakdown, we employed a metaproteomic analysis of extracellular proteins, accomplished by an affinity tagging process using a membrane-impermeable biotinylation tag [64]

Summary

Introduction

Salt marshes are highly productive intertidal ecosystems that generate an abundance of organic carbon in the form of lignocellulose, where net aerial primary productivity often exceeds 1–2 kg C m−2 year−1 [1,2,3]. Mineral protection and preferential retention of recalcitrant organic carbon are major themes governing carbon sequestration [16]; throughout this natural biogeochemical carbon processing, microbial mechanisms of carbon transformation are present and likely operate as a system-level decomposition process that influences the permanence of lignocellulose and stored carbon in marsh sediments. This process is orchestrated by an undefined consortium of organisms prior to entry into stable deeper sediments where this material persists for millennia [6, 17]. We applied meta-exo-proteome proteomics and 16S rRNA gene profiling to study lignocellulose decomposition in situ within the surface level sediments of a natural established UK salt marsh

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Conclusion