Metabolic Exchange with Non-Alkane-Consuming Pseudomonas stutzeri SLG510A3-8 Improves n -Alkane Biodegradation by the Alkane Degrader Dietzia sp. Strain DQ12-45-1b

Abstract

Biodegradation of alkanes by microbial communities is ubiquitous in nature. Interestingly, the microbial communities with high hydrocarbon-degrading performances are sometimes composed of not only hydrocarbon degraders but also nonconsumers, but the synergistic mechanisms remain unknown. Here, we found that two bacterial strains isolated from Chinese oil fields, Dietzia sp. strain DQ12-45-1b and Pseudomonas stutzeri SLG510A3-8, had a synergistic effect on hexadecane (C16 compound) biodegradation, even though P. stutzeri could not utilize C16 individually. To gain a better understanding of the roles of the alkane nonconsumer P. stutzeri in the C16-degrading consortium, we reconstructed a two-species stoichiometric metabolic model, iBH1908, and integrated in silico prediction with the following in vitro validation, a comparative proteomics analysis, and extracellular metabolomic detection. Metabolic interactions between P. stutzeri and Dietzia sp. were successfully revealed to have importance in efficient C16 degradation. In the process, P. stutzeri survived on C16 metabolic intermediates from Dietzia sp., including hexadecanoate, 3-hydroxybutanoate, and α-ketoglutarate. In return, P. stutzeri reorganized its metabolic flux distribution to fed back acetate and glutamate to Dietzia sp. to enhance its C16 degradation efficiency by improving Dietzia cell accumulation and by regulating the expression of Dietzia succinate dehydrogenase. By using the synergistic microbial consortium of Dietzia sp. and P. stutzeri with the addition of the in silico-predicted key exchanged metabolites, diesel oil was effectively disposed of in 15 days with a removal fraction of 85.54% ± 6.42%, leaving small amounts of C15 to C20 isomers. Our finding provides a novel microbial assembling mode for efficient bioremediation or chemical production in the future. IMPORTANCE Many natural and synthetic microbial communities are composed of not only species whose biological properties are consistent with their corresponding communities but also ones whose chemophysical characteristics do not directly contribute to the performance of their communities. Even though the latter species are often essential to the microbial communities, their roles are unclear. Here, by investigation of an artificial two-member microbial consortium in n-alkane biodegradation, we showed that the microbial member without the n-alkane-degrading capability had a cross-feeding interaction with and metabolic regulation to the leading member for the synergistic n-alkane biodegradation. Our study improves the current understanding of microbial interactions. Because “assistant” microbes showed importance in communities in addition to the functional microbes, our findings also suggest a useful “assistant-microbe” principle in the design of microbial communities for either bioremediation or chemical production.

Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery

“…DQ12‐45‐1b from Corynebacteriales and proved the iron‐loaded MVs are shared between species. DQ12‐45‐1b has been reported as actively conducting metabolic exchange with other species (Hu et al ., 2020). Therefore, it is likely that in addition to iron, MVs may participate in the interspecies transport of various molecules, which would strengthen the stress resistance and fitness of microbes in the wider community.…”

“…In addition, DQ12‐45‐1b was able to adapt to multiple stressors including growth at pH 12 and tolerance of NaCl up to a concentration of 20% (Fang et al ., 2018). Recently, we identified active interspecies interactions between DQ12‐45‐1b and P. stutzeri , resulting in enhanced n ‐alkane biodegradation (Hu et al ., 2015; Hu et al ., 2020). However, neither MVs nor their physiological and ecological functions had yet been identified from this species.…”

Biodiversidad bacteriana presente en suelos contaminados con hidrocarburos para realizar biorremediación

“…Este grupo de alcanos es la fracción más volátil del crudo y susceptible a pérdidas abióticas. La exposición prolongada, puede causar dermatitis o cáncer de piel (Coll Almela, 2021;Hu et al, 2020).…”

Comparative transcriptome analysis reveals different adaptation mechanisms for degradation of very long‐chain and normal long‐chain alkanes in Dietzia sp. DQ12‐45‐1b

“…For n-alkane-degrading experiments, DQ12-45-1b cells cultured in GPY medium at 30 C for 36 h (at mid exponential phase) were centrifuged and washed three times with minimal medium (Bihari et al, 2011;Hu et al, 2020). Cells were then cultured in minimal medium with 0.1% (v/v) n-hexadecane (C16), 0.1% (m/v) n-octacosane (C28), and 0.2% (m/v) glucose as the sole carbon (Sabirova et al, 2011;Kothari et al, 2016;Schubeis et al, 2020).…”