Nitrogen Acquisition Strategies Mediated by Insect Symbionts: A Review of Their Mechanisms, Methodologies, and Case Studies

Abstract

Nitrogen is usually a restrictive nutrient that affects the growth and development of insects, especially of those living in low nitrogen nutrient niches. In response to the low nitrogen stress, insects have gradually developed symbiont-based stress response strategies—biological nitrogen fixation and nitrogenous waste recycling—to optimize dietary nitrogen intake. Based on the above two patterns, atmospheric nitrogen or nitrogenous waste (e.g., uric acid, urea) is converted into ammonia, which in turn is incorporated into the organism via the glutamine synthetase and glutamate synthase pathways. This review summarized the reaction mechanisms, conventional research methods and the various applications of biological nitrogen fixation and nitrogenous waste recycling strategies. Further, we compared the bio-reaction characteristics and conditions of two strategies, then proposed a model for nitrogen provisioning based on different strategies.

Gut symbiotic bacteria are involved in nitrogen recycling in the tephritid fruit fly Bactrocera dorsalis

“…Moreover, the limitations of nitrogenase, including extreme oxygen sensitivity, poor catalytic activity and complicated components also weaken the universal applicability of BNF in most living organisms [ 46 , 67 ]. By comparison, NWR appears to be a relatively economical investment in many organisms [ 68 ]. Taking uric acid degradation in termites as an example, the net energy consumption in the de novo synthesis of one molecule of uric acid is only two molecules of MgATP.…”

Bitter friends are not always toxic: The loss of acetic acid bacteria and the absence of Komagataeibacter in the gut microbiota of the polyphagous fly Anastrepha ludens could inhibit its development in Psidium guajava in contrast to A. striata and A. fraterculus that flourish in this host

“…The apparent critical role of the Enterobacteriaceae/Acetobacteraceae ratio in the fitness in the of the three tephritid flies studied represents an interesting phenomenon. Many insects that develop in hosts with high C:N ratios overcome the nitrogen deficiency via their gut microbiota ( Bar-Shmuel et al, 2020 ; Ren et al, 2022 ). The gut microbiota can make the nitrogen available to the insect host via biological nitrogen fixation (BNF), where nitrogen-fixing bacteria, using the nitrogenase complex can transform the atmospheric dinitrogen into ammonia, which can be later assimilated as the non-essential amino acids glutamine and glutamate ( Kneip et al, 2007 ; Ren et al, 2022 ).…”

“…Many insects that develop in hosts with high C:N ratios overcome the nitrogen deficiency via their gut microbiota ( Bar-Shmuel et al, 2020 ; Ren et al, 2022 ). The gut microbiota can make the nitrogen available to the insect host via biological nitrogen fixation (BNF), where nitrogen-fixing bacteria, using the nitrogenase complex can transform the atmospheric dinitrogen into ammonia, which can be later assimilated as the non-essential amino acids glutamine and glutamate ( Kneip et al, 2007 ; Ren et al, 2022 ). This type of symbiosis has been reported in the tephritid flies Ceratitis capitata and Bactrocera tryoni , involving bacteria of the genera Enterobacter and Klebsiella ( Murphy et al, 1994 ; Behar et al, 2005 ).…”

Nutrient-mediated modulation of flowering time

“…Therefore, Fe and S may also regulate plant flowering time through FNR1. Recent studies have mainly focused on the absorption, translocation, and reuse of nutrients ( Verma et al., 2021 ; Wani et al., 2021 ; Johnson et al., 2022 ; Lambers, 2022 ; Liu et al., 2022a ; Liu et al., 2022b ; Podar and Maathuis, 2022 ; Prathap et al., 2022 ; Ren et al., 2022 ; Vélez-Bermúdez and Schmidt, 2022 ; Xie et al., 2022 ), meaning that the potential mechanisms underlying nutrient-regulated flowering remain largely unknown in plants, especially crops. UV stress, drought, salt, cold, and heat also alter flowering ( Martínez et al., 2004 ; Cho et al., 2017 ; Ionescu et al., 2017 ; Shim and Jang, 2020 ; Preston and Fjellheim, 2022 ).…”