Genome-resolved metagenome and metatranscriptome analyses of thermophilic composting reveal key bacterial players and their metabolic interactions

Lucas Palma Perez Braga,José Salvatore Leister Patané,Livia Maria Silva Moura,Fabio Beltrame Sanchez,Roberta Verciano Pereira,Layla Farage Martins,Aline Maria Da Silva,João Carlos Setubal

doi:10.1186/s12864-021-07957-9

Lucas Palma Perez Braga, José Salvatore Leister Patané + Show 6 more

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https://doi.org/10.1186/s12864-021-07957-9

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Journal: BMC Genomics	Publication Date: Sep 10, 2021
Citations: 17	License type: open-access

Affiliation: Universidade de São Paulo, Instituto Butantan

Abstract

BackgroundComposting is an important technique for environment-friendly degradation of organic material, and is a microbe-driven process. Previous metagenomic studies of composting have presented a general description of the taxonomic and functional diversity of its microbial populations, but they have lacked more specific information on the key organisms that are active during the process.ResultsHere we present and analyze 60 mostly high-quality metagenome-assembled genomes (MAGs) recovered from time-series samples of two thermophilic composting cells, of which 47 are potentially new bacterial species; 24 of those did not have any hits in two public MAG datasets at the 95% average nucleotide identity level. Analyses of gene content and expressed functions based on metatranscriptome data for one of the cells grouped the MAGs in three clusters along the 99-day composting process. By applying metabolic modeling methods, we were able to predict metabolic dependencies between MAGs. These models indicate the importance of coadjuvant bacteria that do not carry out lignocellulose degradation but may contribute to the management of reactive oxygen species and with enzymes that increase bioenergetic efficiency in composting, such as hydrogenases and N2O reductase. Strong metabolic dependencies predicted between MAGs revealed key interactions relying on exchange of H+, NH3, O2 and CO2, as well as glucose, glutamate, succinate, fumarate and others, highlighting the importance of functional stratification and syntrophic interactions during biomass conversion. Our model includes 22 out of 49 MAGs recovered from one composting cell data. Based on this model we highlight that Rhodothermus marinus, Thermobispora bispora and a novel Gammaproteobacterium are dominant players in chemolithotrophic metabolism and cross-feeding interactions.ConclusionsThe results obtained expand our knowledge of the taxonomic and functional diversity of composting bacteria and provide a model of their dynamic metabolic interactions.

Highlights

Composting is an important technique for environment-friendly degradation of organic material, and is a microbe-driven process
Pairwise comparisons (Supplementary Table 2) showed that six Metagenome-Assembled Genome (MAG) recovered from ZC3 metagenomes (ZC3RG05, ZC3RG06, ZC3RG07, ZC3RG08, ZC3RG09 and ZC3RG11) are highly similar to six MAGs recovered from ZC4 metagenomes (ZC4RG21, ZC4RG10, ZC4RG11, ZC4RG09, ZC4RG06 and ZC4RG18, respectively); this level of similarity is what we call ‘MAG redundancy’ further down
Metabolic dependencies based on genome-scale models Based on the results obtained with the correlation analysis using the transcriptional activity profile of MAGs (Fig. 5, Supplementary Table 6, Supplementary Table 12) and the activity of relevant genes (Table 2, Supplementary Tables 9, 10, 11, Fig. 3, and Supplementary Fig. 2), we identified MAGs according to their importance in the different stages of composting and the main functions associated with them (Fig. 6)

Summary

Introduction

Composting is an important technique for environment-friendly degradation of organic material, and is a microbe-driven process. Previous metagenomic studies of composting have presented a general description of the taxonomic and functional diversity of its microbial populations, but they have lacked more specific information on the key organisms that are active during the process. Composting microbes present a remarkable metabolic flexibility and are efficient in breaking down complex organic matter such as lignocellulosic biomass [1, 4, 6]. Syntrophic interactions can involve opportunistic microbes in biomass degrading systems, which are bacteria that do not express or very often lack the required enzymes for biomass degradation, but constitute one important portion of the microbial community, being referred to as ‘sugar cheaters’ [8]

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