Chromosome-level genome
assembly of Chironomus striatipennis Kieffer provides insights
into benthic adaptation and metamorphosis mechanism
Bingxin Guo1,
Jinxian Chen1, Liang Lu2, Li
Wang2, Liqing Wang1, Chenhong
Li2, Wenbing Liu3, Ruilei
Zhang1#
1Enginnering Research Center of Environmental DNA and
Ecological Water Health Assessment, College of Fisheries and life
Science, Shanghai Ocean University, Shanghai 201306, China
2The Lab of Molecular Systematics and Ecology, College
of Fisheries and Life Science, Shanghai Ocean University, Shanghai
201306, China
3Tianjin Key Laboratory of Conservation and
Utilization of Animal Diversity, Tianjin Normal University, Tianjin,
China
#Bingxin Guo and Jinxian Chen contributed equally to this work.
#To whom correspondence should be addressed. Email:rlzhang@shou.edu.cn
Abstract : Chironomid is
the most important macroinvertebrate species in aquatic ecosystem.Chironomus represents the most important genus of the
Chironomidae. However, the species of this genus lack a high-quality
assembled genome. Here, a high-quality chromosome-level assembled genome
of Chironomus striatipennis which is an important model organism
in aquatic ecological detection and toxicological application has been
reported. The assembled genome size of C. striatipennis was
181.84 Mb, with a scaffold N50 value of 54.13 Mb. Furthermore, the
molecular mechanism of adaptive evolution of Chironomid to benthic
environment was elucidated by combining transcriptome data of different
stages. The complete metabolic pathway of Hemoglobin was clarified in C.
striatipennis for the first time to suggests the regulatory mechanism
underlying its adaptation to benthic living. The expansions of CYP450s
gene family related to detoxification explain its tolerance to the harsh
environment. The key gene family, JHAMT, involved in biosynthesis of
juvenile hormone are substantially expanded. The expansion of JHAMT
genes and the regular regulation of juvenile hormone and ecdysone
explain the developmental plasticity of C. striatipennis. In this study,
it was also found that C. striatipennis is more dependent on JNK
signal pathway induced metamorphosis than Drosophila
melanogaster . This study provides some views into genetic basis of
tolerance and adaptation of C. striatipennis to harsh benthic
environments and lays a part of the foundation for the adaptive
evolution of benthic animals.
Keywords
Chironomus striatipennis , genome, benthic adaptation,
metamorphosis mechanism
1 Introduction
In aquatic ecosystem, benthos can directly or indirectly affect the
production of fish or waterfowl (Smith, 2014). In many aquatic
ecosystems the number of chironomid species present may account for at
least 50% of the total macroinvertebrate species recorded (Armitage et
al., 1995) and serve as backbone components of aquatic benthic
ecosystem.
Chironomids are the most ubiquitous and frequently the most abundant
insects in all types of freshwater. Under certain conditions, such as at
low levels of dissolved oxygen, larval chironomid may be the only insect
present in benthic sediments (Armitage et al., 1995). Species richness,
wide distribution and tolerance to adverse conditions make them be
frequently selected as good indicator organisms to detect water
environment and pollution in ecological studies (Goto et al., 2011;
Hinton H E, 1951; Pinder, 1986; Sogame & Kikawada, 2017). Recent
research released the flexibility of Hemoglobin in response to
xenobiotics may play a critical role in adaptive evolution in
chironomids (Ha & Choi, 2008). Therefore, the regulation of heme
metabolic pathway related to hemoglobin activity is particularly
important. Another important factor facilitating to adaptation for
environment is that many detoxification enzyme genes are highly
expressed in chironomid (Kozeretska et al., 2022). Futhermore,
chironomids are holometabolous insects undergoing four distinct stages,
egg, larva, pupa and adult, and the larval stage accounts for the vast
majority of the lifecycle. Specifically, after laying eggs, they hatch
into larva in 1-2 day for most Chironomids; after that, chironomid
experiences a period of pelagic life before settling on substrates,
living benthic; when the external environment and its physiological
conditions are suitable, it metamorphoses and emerges into adults
(Armitage et al., 1995). Therefore, chironomid must be able to adapt to
different living environments and have a set of mechanisms that can
regulate metamorphosis and development. However, neither its biological
mechanism to cope with the complex external environment nor its
regulatory mechanism in the process of metamorphosis and eclosion have
been explored. So combing with life cycle characteristics of chironomid,
we can focus on exploring adaptation of chironomid larva to benthic life
and regulation mechanism of metamorphosis and eclosion.
Using high-quality genome as a “scalpel” will help to probe the
genetic basis of environmental adaptation and metamorphosis in these
species. In the last decade, with the popularization and application of
high-throughput sequencing technology, the genomes of more species have
been released. However, in family chironomidae (Diptera, Insecta), the
genomes of only 8 species have been sequenced and assembled (Cornette et
al., 2016; Kelley et al., 2014; Kutsenko et al., 2014; Sun et al., 2021;
Vicoso & Bachtrog, 2015). In previous researches, the genusChironomus has only scaffold level assembled genome (ncbi), the
precision and accuracy of its genome may not rest content with the
increasingly high standard of experimental research. Meanwihle, it has
been proved that there are great differences between the genomes ofChironomus and other genus in Chironomidae (Cornette et al.,
2015). Therefore, it is essential to obtain a high-quality genome ofChironomus species.
Chironomus striatipennis Kieffer (Diptera: Chironomidae) is
widely distributed in Holarctic, Oriental and Neotropical regions; its
larvae frequently present in oligotrophic to eutrophic freshwater, such
as lakes, swamps, rivers, sewage ditches, fish ponds and rice fields; it
is regarded as an alien species to America derived from Asia by
unintentional human transport (Al-Shami et al., 2012; Amora et al.,
2015; Martin, 2017) (Figure 1). C. striatipennis is widespread in
China (Wang et al., 2020); we had ever found its larvae infected
municipal water systems in several cities in South China. Given ease to
reproduce, short life cycle and the larval stage accounts for most of
life cycle, the species is amenable to being maintained as a laboratory
colony for study of various aspects of its biology and toxicology test
(Lacerda et al., 2014; Platzer-Schltz & Welsch, 1969; Platzer-Schultz,
1970; Wu et al., 2021; Zhang et al., 2019). It is necessary to
understand the genetic mechanism of C. striatipennis for
unraveling chironomid adaptability and tolerance (Neff et al., 2021;
Zhang et al., 2020; Zhang et al., 2021).
In present research, Oxford Nanepore technology and Hi-C technology were
applied to generate a chromosome-level genome assembly of C.
striatipennis Kieffer. Further, combined with transcriptome, the
genetic basis of adaptation to benthic low oxygen substrate were
revealed in chironomid larvae, which will set a foundation for exploring
the evolution direction of macrozoobenthos in the benthic environment.