Living in mangroves: a syntrophic scenario unveiling a resourceful microbiome

Abstract

Background: Mangroves are complex and dynamic coastal ecosystems under frequent fluctuations in physicochemical conditions related to the tidal regime. The frequent variation in organic matter concentration, nutrients, and oxygen availability, among other factors, drives the microbial community composition, favoring syntrophic populations harboring a rich and diverse, stress-driven metabolism. Mangroves are known for their carbon sequestration capability, and their complex and integrated metabolic activity is essential to global biogeochemical cycling. Here, we present a metabolic reconstruction based on the genomic functional capability and flux profile between sympatric MAGs co-assembled from a tropical restored mangrove.

Results: Eleven MAGs were assigned to six Bacteria phyla, all distantly related to the available reference genomes. The metabolic reconstruction showed several potential coupling points and shortcuts between complementary routes and predicted syntrophic interactions. Two metabolic scenarios were drawn: a heterotrophic scenario with plenty of carbon sources and an autotrophic scenario with limited carbon sources or under inhibitory conditions. The sulfur cycle was dominant over methane and the major pathways identified were acetate oxidation coupled to sulfate reduction, heterotrophic acetogenesis coupled to carbohydrate catabolism, ethanol production and carbon fixation. Interestingly, several gene sets and metabolic routes similar to those described for wastewater and organic effluent treatment processes were identified.

Conclusion: The mangrove microbial community metabolic reconstruction reflected the flexibility required to survive in fluctuating environments as the microhabitats created by the tidal regime in mangrove sediments. The metabolic components related to wastewater and organic effluent treatment processes identified strongly suggest that mangrove microbial communities could represent a resourceful microbial model for biotechnological applications that occur naturally in the environment.

Keywords: Coastal sediment; MAG; Metabolic reconstruction; Metagenomics; Microbial metabolism.

Fig. 1

Phylogenomic reconstruction of the 11 ETDI MAGs and their evolutionary relationships with public reference genomes. Colored boxes represent the occurrence of that pathway/route/protein in the respective MAG

Fig. 2

General overview of mangroves major pathways identified among the eleven high and medium-high ETDI MAGs. Circles and ellipses represent occurrences of each MAG in each route or step. This figure represents the metabolism as a whole, not schematized under the determination of space and time factors. A-H letters represent guides for a better interpretation of the interconnection between the steps and processes of metabolic dynamics occurring in the community according to the references as indicated in the bottom right

Fig. 3

Energy metabolism. A: sulfur metabolism, B: nitrogen metabolism, C: ATP synthesis, D: proton pumps

Fig. 4

The glycolytic pathway and connections

Fig. 5

TCA cycle, variations and connections

Fig. 6

Volatile fatty acids production and oxidation, and fatty acid degradation: A: acetate, B: propanoate, C: butanoate, D: beta-oxidation, E: alkane degradation, F: benzoyl-CoA degradation