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Mucoromycotina Fungi Possess the Ability to Utilize Plant Sucrose as a Carbon Source: Evidence From Gongronella sp. w5.

ABSTRACT: Mucoromycotina is one of the earliest fungi to establish a mutualistic relationship with plants in the ancient land. However, the detailed information on their carbon supply from the host plants is largely unknown. In this research, a free-living Mucoromycotina called Gongronella sp. w5 (w5) was employed to explore its effect on Medicago truncatula growth and carbon source utilization from its host plant during the interaction process. W5 promoted M. truncatula growth and caused the sucrose accumulation in M. truncatula root tissue at 16 days post-inoculation (dpi). The transportation of photosynthetic product sucrose to the rhizosphere by M. truncatula root cells seemed accelerated by upregulating the SWEET gene. A predicted cytoplasmic invertase (GspInv) gene and a sucrose transporter (GspSUT1) homology gene in the w5 genome upregulated significantly at the transcriptional level during w5-M. truncatula interaction at 16 dpi, indicating the possibility of utilizing plant sucrose directly by w5 as the carbon source. Further investigation showed that the purified GspInv displayed an optimal pH of 5.0 and a specific activity of 3380 ± 26 U/mg toward sucrose. The heterologous expression of GspInv and GspSUT1 in Saccharomyces cerevisiae confirmed the function of GspInv as invertase and GspSUT1 as sugar transporter with high affinity to sucrose in vivo. Phylogenetic tree analysis showed that the ability of Mucoromycotina to utilize sucrose from its host plant underwent a process of "loss and gain." These results demonstrated the capacity of Mucoromycotina to interact with extant land higher plants and may employ a novel strategy of directly up-taking and assimilating sucrose from the host plant during the interaction.

SUBMITTER: Wang X

PROVIDER: S-EPMC7874188 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Proteins in the Glycoside Hydrolase family 32 (GH32) are carbohydrate-active enzymes known as invertases that hydrolyse the glycosidic bonds of complex saccharides. Fungi rely on these enzymes to gain access to and utilize plant-derived sucrose. In fungi, GH32 invertase genes are found in higher copy numbers in the genomes of pathogens when compared to closely related saprophytes, suggesting an association between invertases and ecological strategy. The aim of this study was to investigate the distribution and evolution of GH32 invertases in the Ceratocystidaceae using a comparative genomics approach. This fungal family provides an interesting model to study the evolution of these genes, because it includes economically important pathogenic species such as Ceratocystis fimbriata, C. manginecans and C. albifundus, as well as saprophytic species such as Huntiella moniliformis, H. omanensis and H. savannae. RESULTS:The publicly available Ceratocystidaceae genome sequences, as well as the H. savannae genome sequenced here, allowed for the identification of novel GH32-like sequences. The de novo assembly of the H. savannae draft genome consisted of 28.54 megabases that coded for 7 687 putative genes of which one represented a GH32 family member. The number of GH32 gene family members appeared to be related to the ecological adaptations of these fungi. The pathogenic Ceratocystis species all contained two GH32 family genes (a putative cell wall and a putative vacuolar invertase), while the saprophytic Huntiella species had only one of these genes (a putative cell wall invertase). Further analysis showed that the evolution of the GH32 gene family in the Ceratocystidaceae involved transposable element-based retro-transposition and translocation. As an example, the activity of a Fot5-like element likely facilitated the assembly of the genomic regions harbouring the GH32 family genes in Ceratocystis. CONCLUSIONS:This study provides insight into the evolutionary history of the GH32 gene family in Ceratocystidaceae. Our findings suggest that transposable elements shaped the evolution of the GH32 gene family, which in turn determines the sucrolytic activities and related ecological strategies of the Ceratocystidaceae species that harbour them. The study also provides insights into the role of carbohydrate-active enzymes in plant-fungal interactions and adds to our understanding of the evolution of these enzymes and their role in the life style of these fungi.

Project description:Most strains of Vibrio parahaemolyticus are unable to utilize sucrose as carbon source, though few exceptions exist. We investigated a sucrose-positive V. parahaemolyticus strain by whole-genome sequencing (WGS) and confirmed the presences of a genomic island containing sucrose utilization genes. A 4.7 kb DNA cluster consisting of three genes: scrA encoding a sucrose uptake protein, scrK encoding a fructokinase, and scrB coding for a sucrose-6-phosphate hydrolase, was PCR amplified and inserted into the Vibrio/Escherichia coli shuttle vector pVv3. Two recombinant plasmids, only differing in the orientation of the insert with respect to the pVv3-lacZα-fragment, conferred the E. coli K12 transformants the ability to utilize sucrose. The introduction of the two plasmids into sucrose-negative V. parahaemolyticus and V. vulnificus strains also results in a change of the sucrose utilization phenotype from negative to positive. By performing a multiplex PCR targeting scrA, scrK, and scrB, 43 scr-positive V. parahaemolyticus isolates from our collection of retail strains were detected and confirmed to be able to use sucrose as carbon source. Strains unable to utilize the disaccharide were negative by PCR for the scr genes. For in-depth characterization, 17 sucrose-positive V. parahaemolyticus were subjected to WGS. A genomic island with a nucleotide identity of >95% containing scrA, scrB, scrK and three additional coding sequences (CDS) were identified in all strains. The additional genes were predicted as a gene coding for a transcriptional regulator (scrR), a porin encoding gene and a CDS of unknown function. Sequence comparison indicated that the genomic island was located in the same region of the chromosome II in all analyzed V. parahaemolyticus strains. Structural comparison of the genomes with sequences of the sucrose utilizing species V. alginolyticus revealed the same genomic island, which indicates a possible distribution of this genetic structure by horizontal gene transfer. The comparison of all genome sequences based on SNP differences reveals that the presence of sucrose utilizing genes is found in genetically diverse V. parahaemolyticus strains and is not restricted to a subset of closely related strains.

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Mucoromycotina Fungi Possess the Ability to Utilize Plant Sucrose as a Carbon Source: Evidence From Gongronella sp. w5.

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