Metatranscriptomic Analysis of the Bacterial Symbiont Dactylopiibacterium carminicum from the Carmine Cochineal Dactylopius coccus (Hemiptera: Coccoidea: Dactylopiidae)

Abstract

The scale insect Dactylopius coccus produces high amounts of carminic acid, which has historically been used as a pigment by pre-Hispanic American cultures. Nowadays carmine is found in food, cosmetics, and textiles. Metagenomic approaches revealed that Dactylopius spp. cochineals contain two Wolbachia strains, a betaproteobacterium named Candidatus Dactylopiibacterium carminicum and Spiroplasma, in addition to different fungi. We describe here a transcriptomic analysis indicating that Dactylopiibacterium is metabolically active inside the insect host, and estimate that there are over twice as many Dactylopiibacterium cells in the hemolymph than in the gut, with even fewer in the ovary. Albeit scarce, the transcripts in the ovaries support the presence of Dactylopiibacterium in this tissue and a vertical mode of transmission. In the cochineal, Dactylopiibacterium may catabolize plant polysaccharides, and be active in carbon and nitrogen provisioning through its degradative activity and by fixing nitrogen. In most insects, nitrogen-fixing bacteria are found in the gut, but in this study they are shown to occur in the hemolymph, probably delivering essential amino acids and riboflavin to the host from nitrogen substrates derived from nitrogen fixation.

Cultivable, Host-Specific Bacteroidetes Symbionts Exhibit Diverse Polysaccharolytic Strategies

“…2A and B and 3A). Given that P. americana lacks endogenous pectinases, pectinolytic gut symbionts may be relied upon to supply the enzymes necessary for deconstructing this abundant dietary component, as observed in honey bees (Apis mellifera) and scale insects (Dactylopius coccus) (60,61). In B. thetaiotaomicron, dietary pectic glycans are degraded by PULs catabolizing galactan, arabinan, homogalacturonan (HG), and rhamnogalacturonan I (RGI) (8).…”

Insight into the bacterial communities of the subterranean aphid Anoecia corni

“…One OTU was assigned to D. carminicum (β-proteobacteria, family Rhodocyclaceae). So far, this bacterial species has only been reported in the scale insect species Dactylopius coccus (Hemiptera: Coccoidea: Dactylopiidae), where it has been described as a nitrogen-fixing symbiont [103,104]. Dactylopius coccus is now well established in Morocco where it ravages the plants of Opuntia ficus-indica.…”

We and herbivores eat endophytes

“…In sapsucking insects, protease activity was found in guts and it was suggested that 'digestive proteolysis may be widespread in homoptera' (Foissac et al, 2002). In the carmine cochineal, Dactylopiibacterium showed increased expression of protease and peptidase genes in a gut metatranscriptomic analysis suggesting a bacterial origin of proteases in guts (Bustamante-Brito et al, 2019). Some herbivores have a specialized diet, for example koalas eat eucalyptus, pandas eat bamboos, tortoises eat cactus, Monarch butterfly pupas eat Asclepias and maguey red worms eat Agave cactuses and their microbiota serves to digest some of the particular substances or antimetabolites in their host plants.…”

“…In sap‐sucking insects, protease activity was found in guts and it was suggested that ‘digestive proteolysis may be widespread in homoptera’ (Foissac et al , 2002). In the carmine cochineal, Dactylopiibacterium showed increased expression of protease and peptidase genes in a gut metatranscriptomic analysis suggesting a bacterial origin of proteases in guts (Bustamante‐Brito et al , 2019).…”

“…Further metagenomic studies of D. coccus and D. opuntiae allowed us to obtain the genome of a betaproteobacterium ( Dactylopiibacterium carminicum ) related to the grass endophytes Uliginosibacterium and Azoarcus (Vera‐Ponce de León et al , 2017). Several characteristics of Dactylopiibacterium remind endophytes, like the ability to fix atmospheric nitrogen, to produce cellulases and pectinases, and to catabolize salicylic acid that is produced in plants (Vera‐Ponce de Leon et al 2017; Bustamante‐Brito et al , 2019). Our results suggested an endophytic origin of Dactylopiibacterium symbionts.…”