Iron is not everything: unexpected complex metabolic responses between iron-cycling microorganisms

• Published in: The ISME Journal Vol. 14; no. 11; pp. 2675 - 2690
• Main Authors: Cooper, Rebecca E., Wegner, Carl-Eric, Kügler, Stefan, Poulin, Remington X., Ueberschaar, Nico, Wurlitzer, Jens D., Stettin, Daniel, Wichard, Thomas, Pohnert, Georg, Küsel, Kirsten
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.11.2020
• Subjects: 38/39; 45/22; 45/77; 45/90; 45/91; 631/158/855; 631/326/47; 82/16; Biomedical and Life Sciences; Ecology; Evolutionary Biology; Ferrous Compounds; Gallionellaceae; Iron; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Oxidation-Reduction; Shewanella - genetics
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/s41396-020-0718-z

Coexistence of microaerophilic Fe(II)-oxidizers and anaerobic Fe(III)-reducers in environments with fluctuating redox conditions is a prime example of mutualism, in which both partners benefit from the sustained Fe-pool. Consequently, the Fe-cycling machineries (i.e., metal-reducing or –oxidizing pathways) should be most affected during co-cultivation. However, contrasting growth requirements impeded systematic elucidation of their interactions. To disentangle underlying interaction mechanisms, we established a suboxic co-culture system of Sideroxydans sp. CL21 and Shewanella oneidensis . We showed that addition of the partner’s cell-free supernatant enhanced both growth and Fe(II)-oxidizing or Fe(III)-reducing activity of each partner. Metabolites of the exometabolome of Sideroxydans sp. CL21 are generally upregulated if stimulated with the partner´s spent medium, while S. oneidensis exhibits a mixed metabolic response in accordance with a balanced response to the partner. Surprisingly, RNA-seq analysis revealed genes involved in Fe-cycling were not differentially expressed during co-cultivation. Instead, the most differentially upregulated genes included those encoding for biopolymer production, lipoprotein transport, putrescine biosynthesis, and amino acid degradation suggesting a regulated inter-species biofilm formation. Furthermore, the upregulation of hydrogenases in Sideroxydans sp. CL21 points to competition for H 2 as electron donor. Our findings reveal that a complex metabolic and transcriptomic response, but not accelerated formation of Fe-end products, drive interactions of Fe-cycling microorganisms.