Defining the eco-enzymological role of the fungal strain Coniochaeta sp. 2T2.1 in a tripartite lignocellulolytic microbial consortium

Authors: JIMENEZ, DIEGO JAVIER - Universidad De Los Andes; WANG, YANFANG - University Of Groningen; DE MARES, MARYAM CHAIB - University Of Groningen; CORTES-TOLALPA, LARISA - University Of Groningen; Mertens, Jeffrey; Hector, Ronald - Ron; LIN, JUNYAN - Department Of Energy Joint Genome; JOHNSON, JENIFER - Department Of Energy Joint Genome; LIPZEN, ANNA - Department Of Energy Joint Genome; BARRY, KERRIE - Department Of Energy Joint Genome; MONDO, STEPHEN - Department Of Energy Joint Genome; GRIGORIEV, IGOR - Department Of Energy Joint Genome; Nichols, Nancy; VAN ELSAS, JAN DIRK - University Of Groningen

Submitted to: FEMS Microbiology Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/22/2019
Publication Date: 11/26/2019
Citation: Jimenez, D., Wang, Y., de Mares, M., Cortes-Tolalpa, L., Mertens, J.A., Hector, R.E., Lin, J., Johnson, J., Lipzen, A., Barry, K., Mondo, S.J., Grigoriev, I.V., Nichols, N.N., Van Elsas, J.D. 2019. Defining the eco-enzymological role of the fungal strain Coniochaeta sp. 2T2.1 in a tripartite lignocellulolytic microbial consortium. FEMS Microbiology Ecology. 96(1). Article fiz186. https://doi.org/10.1093/femsec/fiz186.
DOI: https://doi.org/10.1093/femsec/fiz186

Interpretive Summary: A major challenge to producing commodity biofuels and chemicals from agricultural residues is the need to break down the biomass to simple sugars. In nature, plant decay is carried out by microbes that produce enzymes to degrade the fibrous material. Due to the complexity of the fibers in plant biomass, a multitude of enzymes secreted by a mixture of microbes is involved in the process. Research efforts in biorefining are directed at mimicking the natural process, in order to efficiently liberate usable sugars from plant residues. We put together a mixture of microbes to break down wheat straw and probed the role of each member of the consortium. A soil fungus named 2T2.1 has an exceptional array of genes for degradation of plant material. When the fungus was mixed with two types of bacteria and grown on wheat straw, the fungus produced enzymes to degrade plant lignin. The bacteria could complement the breakdown of lignin, having activities to degrade other types of plant fibers. In addition, more than 50 new genes related to biomass breakdown were identified. Understanding the function of the new genes may lead to new applications in biotechnology and inclusion of these activities in enzyme cocktails could improve the biorefining process to utilize agricultural residues.

Technical Abstract: Coniochaeta species are versatile ascomycetes that have great capacity to deconstruct lignocellulose. Here, we explored the transcriptome of Coniochaeta sp. strain 2T2.1 from wheat straw-driven cultures with the fungus grown alone or as a member of a mixed synthetic consortium with Sphingobacterium multivorum w15 and Citrobacter freundii so4. The differential expression profiles of carbohydrate-active enzymes indicated an onset of wheat straw degradation by 2T2.1 during the initial 24 hours of incubation. Expression levels for 63 and 62 genes were significantly different at 24 and 72 hours of cultivation, respectively. Interestingly, the presence of the two bacteria significantly upregulated the expression of one laccase-like enzyme (~ 437 fold at 24 hours), two bilirubin oxidases and one beta-glucuronidase. The laccase-like protein (family AA1_3) had ~75% similarity with a multicopper oxidase of Meliniomyces bicolor, and conserved histidine residues of the copper-binding motifs were identified. The data indicate that 2T2.1 may be involved in lignin transformations, while S. multivorum and C. freundii have the metabolic potential to deconstruct arabinoxylan. Under the conditions applied, 2T2.1 appears to be a better deconstructor of lignocellulose when the two bacteria are absent. This conclusion is supported by the suppression of its (hemi)cellulolytic arsenal and the lower degradation rates within the tripartite consortium.