Huanglongbing alters the structure and functional diversity of microbial communities associated with citrus rhizosphere

Abstract

The diversity and stability of bacterial communities present in the rhizosphere heavily influence soil and plant quality and ecosystem sustainability. The goal of this study is to understand how ‘Candidatus Liberibacter asiaticus’ (known to cause Huanglongbing, HLB) influences the structure and functional potential of microbial communities associated with the citrus rhizosphere. Clone library sequencing and taxon/group-specific quantitative real-time PCR results showed that ‘Ca. L. asiaticus’ infection restructured the native microbial community associated with citrus rhizosphere. Within the bacterial community, phylum Proteobacteria with various genera typically known as successful rhizosphere colonizers were significantly greater in clone libraries from healthy samples, whereas phylum Acidobacteria, Actinobacteria and Firmicutes, typically more dominant in the bulk soil were higher in ‘Ca. L. asiaticus’-infected samples. A comprehensive functional microarray GeoChip 3.0 was used to determine the effects of ‘Ca. L. asiaticus’ infection on the functional diversity of rhizosphere microbial communities. GeoChip analysis showed that HLB disease has significant effects on various functional guilds of bacteria. Many genes involved in key ecological processes such as nitrogen cycling, carbon fixation, phosphorus utilization, metal homeostasis and resistance were significantly greater in healthy than in the ‘Ca. L. asiaticus’-infected citrus rhizosphere. Our results showed that the microbial community of the ‘Ca. L. asiaticus’-infected citrus rhizosphere has shifted away from using more easily degraded sources of carbon to the more recalcitrant forms. Overall, our study provides evidence that the change in plant physiology mediated by ‘Ca. L. asiaticus’ infection could elicit shifts in the composition and functional potential of rhizosphere microbial communities. In the long term, these fluctuations might have important implications for the productivity and sustainability of citrus-producing agro-ecosystems.

Defining the Core Citrus Leaf- and Root-Associated Microbiota: Factors Associated with Community Structure and Implications for Managing Huanglongbing (Citrus Greening) Disease

“…A growing number of studies have focused on understanding how the plant microbiome changes during disease development (15,17,(20)(21)(22)(23)(24)(25)(26). While results from these studies suggest that plant-associated microbial communities undergo perturbation during environmental change or disease progression, one may alternatively argue that the disease itself is a consequence of complex changes to the communities.…”

“…As for root microbiota, the declining health state of the trees may have altered the composition and amounts of root exudates produced. Trivedi et al (24) reported HLB infection significantly alters the abundances of functional genes in the citrus rhizosphere that are involved in carbon fixation, nitrogen cycling, phosphorus utilization, and metal homeostasis, which reflected a state of environmental change. On the other hand, since the relative abundance of Liberibacter spp.…”

“…Understanding the importance of the core group with regard to its implications for plant health and productivity is still at a stage of infancy. Plant diseases are known to be associated with changes in the microbiome (15,17,(20)(21)(22)(23)(24)(25)(26), but much remains to be learned about potential interactions between phytopathogens and native bacteria, notably core microbiota, that could play key roles in disease progression. The present study investigated these associations and interactions through a comprehensive analysis of the core leaf-and root-associated communities of citrus hosts that varied in the extent of HLB disease progression.…”

Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships

“…Quantitative PCR (qPCR) qPCR was performed to determine gene copy numbers for bacteria and fungi, including α-Proteobacteria, β-Proteobacteria, Fimiricutes, Actinobacteria, Acidobacteria and Basidiomycota, using the primers and conditions described previously by Trivedi et al (2012). Spearman correlation analyses were performed by using the XLSTAT software (Addinsoft SARL, Paris, France) to test the relationship between relative abundance determined by qPCR and the relative abundance determined by pyrosequencing.…”

High Incidence of Preharvest Colonization of Huanglongbing-Symptomatic Citrus sinensis Fruit by Lasiodiplodia theobromae (Diplodia natalensis) and Exacerbation of Postharvest Fruit Decay by That Fungus

“…HLB not only affects plant health but can also alter the structure and composition of bacterial communities associated with citrus leaves (6), roots (7), and rhizospheres (8). In our investigation conducted to identify fungal species in orange juice from HLB-symptomatic ("Ca.…”