Abstract

Diverse physiological groups congregate into environmental corrosive biofilms, yet the interspecies interactions between these corrosive physiological groups are seldom examined. We, therefore, explored Fe0-dependent cross-group interactions between acetogens and methanogens from lake sediments. On Fe0, acetogens were more corrosive and metabolically active when decoupled from methanogens, whereas methanogens were more metabolically active when coupled with acetogens. This suggests an opportunistic (win–loss) interaction on Fe0 between acetogens (loss) and methanogens (win). Clostridia and Methanobacterium were the major candidates doing acetogenesis and methanogenesis after four transfers (metagenome sequencing) and the only groups detected after 11 transfers (amplicon sequencing) on Fe0. Since abiotic H2 failed to explain the high metabolic rates on Fe0, we examined whether cell exudates (spent media filtrate) promoted the H2-evolving reaction on Fe0 above abiotic controls. Undeniably, spent media filtrate generated three- to four-fold more H2 than abiotic controls, which could be partly explained by thermolabile enzymes and partly by non-thermolabile constituents released by cells. Next, we examined the metagenome for candidate enzymes/shuttles that could catalyze H2 evolution from Fe0 and found candidate H2-evolving hydrogenases and an almost complete pathway for flavin biosynthesis in Clostridium. Clostridial ferredoxin-dependent [FeFe]-hydrogenases may be catalyzing the H2-evolving reaction on Fe0, explaining the significant H2 evolved by spent media exposed to Fe0. It is typical of Clostridia to secrete enzymes and other small molecules for lytic purposes. Here, they may secrete such molecules to enhance their own electron uptake from extracellular electron donors but indirectly make their H2-consuming neighbors—Methanobacterium—fare five times better in their presence. The particular enzymes and constituents promoting H2 evolution from Fe0 remain to be determined. However, we postulate that in a static environment like corrosive crust biofilms in lake sediments, less corrosive methanogens like Methanobacterium could extend corrosion long after acetogenesis ceased, by exploiting the constituents secreted by acetogens.

Highlights

  • Steel infrastructure extends for billions of kilometers below ground enabling transport and storage of clean water, chemicals, fuels, and sewage, and protection for telecommunication and electricity cables

  • Methanogens When the corrosive community reached the fourth transfer on Fe0, using shotgun metagenomics, we identified two major methanogenic groups: Methanomicrobia (48% of Archaea; 3.2% of assembled prokaryotic reads, 1 assembled bin) and Methanobacteria (38.5% of Archaea; 2.6% of assembled prokaryotic reads, 1 assembled bin)

  • We found no evidence in the metagenome that methanogens had the potential to accelerate electron uptake from Fe0 as they did not present the microbial-induced corrosion (MIC) island specific to highly corrosive methanogens (Tsurumaru et al, 2018). [NiFe]-hydrogenases on the MIC island of methanogens promotes corrosion only when encoded on the genomic island (MIC island) between secretory proteins, which apparently help the hydrogenase on its way out of the cell to the extracellular electron donor (Tsurumaru et al, 2018)

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Summary

Introduction

Steel infrastructure extends for billions of kilometers below ground enabling transport and storage of clean water, chemicals, fuels, and sewage, and protection for telecommunication and electricity cables. Urban storm and rainfall management in many countries, especially northern countries like Denmark, involves so-called climate lakes ( known as stormwater ponds or retention ponds) harvesting rainfall at a large scale, alleviating stormwater runoff in the cities (Mishra et al, 2020). It is important to predict the lifespan of the material if exposed to microbial communities native to the site where steel structures are located. This would lead to effective replacement and metal recuperation strategies before accidental spills that may be detrimental to the surrounding environment (Usher et al, 2014a; Skovhus et al, 2017; Arriba-Rodriguez et al, 2018)

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