Starvation Promotes Autophagy-Associated Maturation of the Testis in the Giant Freshwater Prawn, Macrobrachium rosenbergii

Abstract

Autophagy is a degradative process of cellular components accomplished through an autophagosomal-lysosomal pathway. It is an evolutionary conserved mechanism present in all eukaryotic cells, and it plays a fundamental role in maintaining tissue homeostasis both in vertebrates and invertebrates. Autophagy accompanies tissue remodeling during organ differentiation. Several autophagy-related genes and proteins show significant upregulations following nutrient shortage (i.e., starvation). In our previous study, we found that in female giant freshwater prawns subjected to a short period of starvation autophagy was up-regulated in consonant with ovarian maturation and oocyte differentiation. Whether and how starvation-induced autophagy impacts on testicular maturation and spermatogenesis of the male prawns remained to be investigated. In this study, we analyzed the effects of starvation on histological and cellular changes in the testis of the giant freshwater prawn Macrobrachium rosenbergii that paralleled the induction of autophagy. Under short starvation condition, the male prawns showed increased gonado-somatic index, increased size, and late stage of maturation of seminiferous tubules, which contained increased number of spermatozoa. Concurrently, the number of autophagy vacuoles and autophagy flux, as monitored by transmission electron microscopy and the autophagic marker LC3, increased in the testicular cells, indicating that a short period of starvation could induce testicular maturation and spermatogenesis in male M. rosenbergii along with modulation of autophagy.

Regulation of early spermatogenesis in the giant prawn Macrobrachium rosenbergii by a GCL homolog

“…Detailed knowledge of the process of spermatogenesis in M. rosenbergii [ 18 ] has been applied in several studies for spermatogenic staging [ 19 , 20 ] through 12 morphologically distinct stages. From these studies, it is known that the testes display two distinct regions: the region adjacent to the epithelial cells at the periphery of the lobule contains dividing spermatogonia (germline/maturing sperm cells), which begin differentiating into spermatozoa, while the lumen at the center of the lobule contains spermatozoa (mature sperm cells), some still in the process of spermatogenesis.…”

Response of the metabolic and autophagy pathways in Mytilus under starvation

“…Mytilus mainly feed on natural algae and organic debris in the ocean, while starvation is a major problem often encountered in the growth of mussels due to improper feeding, insufficient abundance, uneven spatial distribution, seasonal change or drastic environmental change in natural sea areas (Li et al, 2010). Starvation will not only lead to inadequate nutrition of shellfish, but also affect the weight, metabolism and energy reserves of other aquatic organisms to a certain extent (Dai et al, 2018;Kankuan et al, 2019;Xu et al, 2021). Moreover, imbalance in nutrient supply will also lead to metabolic disorders in aquatic organisms, and eventually shorten the life span of many different organisms (Dai et al, 2018;Kankuan et al, 2019;Xu et al, 2021).…”

“…Starvation will not only lead to inadequate nutrition of shellfish, but also affect the weight, metabolism and energy reserves of other aquatic organisms to a certain extent (Dai et al, 2018;Kankuan et al, 2019;Xu et al, 2021). Moreover, imbalance in nutrient supply will also lead to metabolic disorders in aquatic organisms, and eventually shorten the life span of many different organisms (Dai et al, 2018;Kankuan et al, 2019;Xu et al, 2021). At the same time, starvation stress will affect the adaptability of marine organisms to the aquatic environment, may prolong or even fail to adapt, and may further affect the growth, defense system and reproduction of marine organisms (Mahapatra et al, 2017;Haider et al, 2020).…”