Annotation of detoxification-related gene families
The detoxification of xenobiotics is essential for the environmental
adaptation of arthropods, including collembolans. The expansion of
detoxification-related gene families is often observed in highly
polyphagous species. We manually
annotated ABC, CCE, CYP, GST and UGT genes in the two F. candidastrains (Table 2, Figure 4, Figure S4). In contrast to D.
melanogaster , the ABC, CCE, CYP and GST families were greatly expanded
in the two F. candida strains. FCDK showed greater expansion of
the ABC, CYP and GST families than FCSH, consistent with the wider
distribution of the former strain.
ABC transporters function as primary active transporters that transport
diverse substrates across lipid membranes and include eight subfamilies,
A‒H (Dermauw & Van Leeuwen, 2014). The gene numbers of ABCB, ABCD, ABCE
and ABCF subfamilies are similar among FCDK, FCSH and D .melanogaster (Table 2, Figure 4a). D. melanogaster shows
the fewest ABCG and ABCH genes but the greatest number of ABCA genes,
which are related to lipid trafficking (Wenzel et al., 2007). ABCG genes
exhibit diverse functions in eye colouration determination (Ewart et
al., 1994; Mackenzie et al., 1999), moulting hormone regulation (Hock et
al., 2000; Broehan et al., 2013) and xenobiotic resistance (Labbé et
al., 2011). In contrast to FCSH, FCDK shows a major expansion of ABCC
subfamily, which are functionally diverse, playing roles in processes
comprising ion transport, cell-surface receptor activity and the
translocation of a broad range of substrates (Dean et al., 2001; Kruh &
Belinsky, 2003; Moreau et al., 2005).
CCEs hydrolysing carboxylic esters can be classified into three larger
classes: dietary/detoxification, hormone/semiochemical processing and
neurodevelopmental functions (Oakeshott et al., 2005).
Dietary/detoxification CCEs accounted for 2/3 of all annotated CCEs in
FCDK and FCSH. The two F. candida strains possessed five times as
many dietary/detoxification-related and two times as many
hormone/semiochemical CCEs as D. melanogaster (Table 2). No
significant difference in CCE copy numbers was observed between FCDK and
FCSH (Figure S4a).
The CYP superfamily is one of the most groups of important xenobiotic
metabolism enzymes in arthropods and is usually classified into CYP2,
CYP3, CYP4 and mitochondrial clans (Feyereisen 2006, 2012). For the CYPs
identified in both F. candida strains, approximately 1/2 of the
genes were clustered into the CYP2 clan, whereas few genes were included
in the mitochondrial clan (Table 2, Figure 4b). The large number of CYP2
genes found in F. candida was similar to that reported in
Chelicerata (Grbić et al., 2011; Fan et al., 2021) but different from
that in insects. CYP2 enzymes are associated with the detoxification and
bioactivation of certain exogenous chemicals (Feyereisen 2006). An
obvious expansion of the clan CYP3 was also observed in FCDK and FCSH;
these enzymes have been found to be major participants associated with
xenobiotic metabolism and insecticide resistance across a wide range of
artificial or natural chemicals. FCSH showed a contraction in the CYP4
clan relative to FCDK and D. melanogaster .
GST enzymes play a crucial role in the detoxification of a wide range of
exogenous and endogenous compounds, particularly in insecticide
resistance (Enayati et al., 2005; Li et al., 2007). GSTs can be
classified into three superfamilies: cytosolic (13 classes),
mitochondrial (kappa), and microsomal (MAPEG) (Oakley, 2011). Few
microsomal GSTs were observed, and mitochondrial GSTs were completely
lacking in the three taxa. Seven cytosolic classes were observed, among
which the epsilon class was absent in FCDK and FCSH and mu was absent inD. melanogaster (Table 2, Figure S4b). The GST class pattern
observed in the two F. candida strains strongly conformed to that
observed in noninsect arthropods (Labbé et al., 2011; Roncalli et al.,
2015; Fan et al., 2021). Folsomia showed a great expansion of the
sigma class, which accounted for more than half of the annotated GSTs.
Sigma GSTs have anti- and proinflammatory functions in mammals, immune
response functions in helminth parasites, and lipid oxidation product
detoxification functions in insects (Flanagan & Smythe, 2011).
Insect UGTs have diverse functions, including roles in processes such as
detoxification (Smith, 1955), insecticide resistance (Lee et al., 2005),
pigmentation (Hopkins & Ahmad, 1991), and sclerotization (Hopkins,
1992). FCDK and FCSH each had 48 UGTs, which was slightly greater than
the number in D. melanogaster (Table 2). Most FolsomiaUGTs were clustered into two clades with node support of 100 and were
isolated from D. melanogaster UGTs, indicating an independent
origin of Folsomia UGT families (Figure S4c).