Different feeding habits influence the activity of digestive enzymes in freshwater fish

Gioda, Carolina Rosa; Pretto, Alexandra; Freitas, Carine de Souza; Leitemperger, Jossiele; Loro, Vânia Lúcia; Lazzari, Rafael; Lissner, Leandro Ademar; Baldisserotto, Bernardo; Salbego, Joseânia

doi:10.1590/0103-8478cr20160113

Cited by 27 publications

(18 citation statements)

References 12 publications

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“…Interestingly, C. violaceus appears to express three separate chymotrypsin genes and only one trypsin gene. This may be consistent with their consumption of algal material, as carnivores (e.g., salmon) may invest more in trypsin expression (Rungruangsak-Torrissen et al 2006), whereas herbivores (e.g., grass carp) may express more chymotrypsin (Gioda et al 2017).…”

Section: Transcriptomicsmentioning

confidence: 65%

Physiological genomics of dietary adaptation in a marine herbivorous fish

Heras

Chakraborty

Emerson

et al. 2018

Preprint

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Adopting a new diet is a significant evolutionary change and can profoundly affect an animal's physiology, biochemistry, ecology, and its genome. To study this evolutionary transition, we investigated the physiology and genomics of digestion of a derived herbivorous fish, the monkeyface prickleback (Cebidichthys violaceus). We sequenced and assembled its genome and digestive transcriptome and revealed the molecular changes related to important dietary enzymes, finding abundant evidence for adaptation at the molecular level. In this species, two gene families experienced expansion in copy number and adaptive amino acid substitutions. These families, amylase, and bile salt activated lipase, are involved digestion of carbohydrates and lipids, respectively. Both show elevated levels of gene expression and increased enzyme activity. Because carbohydrates are abundant in the prickleback's diet and lipids are rare, these findings suggest that such dietary specialization involves both exploiting abundant resources and scavenging rare ones, especially essential nutrients, like essential fatty acids. Main Populations exposed to new environments often experience strong natural selection (e.g., Herrel et al. 2008). Comparing closely related species has been an effective perspective in pinpointing changes that drive adaptation (Dasmahapatra et al. 2012; Lamichhaney et al. 2015). In its most powerful incarnation, the comparative method links variation at the genetic level to molecular phenotypes that in turn change how whole organisms interact with their environments, revealing for example adaptation to new abiotic factors (Protas et al. 2006; Chakraborty and Fry 2015; Peichel and Marques 2017; Tong et al. 2017; Chen et al. 2018), changes in diet (Harris and Munshi-South 2017; Hsieh et al. 2017; Zepeda-Mendoza et al. 2018), and exposure to pollution (Vega-Retter et al. 2018). In animals, digestion is an ideal model phenotype because it is central to fitness, is understood in many species at genetic, molecular, biochemical, and physiological levels, and is a trait that shows abundant variation throughout animal evolution (Karasov and Martinez del Rio 2007). While studies of animal digestion have yielded insights into the physiology and biochemistry of adaptation, untangling its genetic basis is contingent on the availability and quality of genomic resources, which have traditionally been lacking in nonmodel species. Advances in genome technology have improved the quality and decreased the cost of obtaining sequences, stimulating the production of genome assemblies and catalyzing genetic discoveries for a diverse array of non-model organisms.Here we describe the genetic changes accompanying acquisition of an herbivorous diet in the marine intertidal fish, Cebidichthys violaceus. To do this we generated a physiological genomics dataset for this non-model species, including a highly contiguous and complete genome, the transcriptomes of digestive and hepatic tissues, and digestive enzyme activity levels.

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Section: Transcriptomicsmentioning

confidence: 65%

Physiological genomics of dietary adaptation in a marine herbivorous fish

Heras

Chakraborty

Emerson

et al. 2018

Preprint

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“…In freshwater fish such as the carnivorous Hoplias malabaricus were reported higher acid protease and trypsin activities, while in herbivorous fish grass carp Ctenopharyngodon idella the higher activity enzymes were amylase and maltase. However, omnivorous species such as piava Leporinus obtusidens and silver catfish Rhamdia quelen showed intermediate activity values (Gioda et al, ). On the other hand, in the long‐whiskered Pimelodus maculatus was reported a hepatic β‐glucosidase activity higher in an oligotrophic reservoir, while the chymotrypsin‐like activity was higher in eutrophic reservoir.…”

Section: Introductionmentioning

confidence: 99%

Expression analyses of digestive enzymes during early development and in adults of the chame fishDormitator latifrons

et al. 2019

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This study describes the expression of genes that encode digestive enzymes (trypsin, pepsinogen, maltase-glucoamylase, sucrase-isomaltase, alkaline phosphatase and leucine aminopeptidase) using qRT-PCR in 0-to 7-day post-hatching (dph) chame (Dormitator latifrons). Additionally, adults liver and intestine were analysed for enzyme expression.Results showed that transcripts for all enzymes are present in both adult and larvae tissues. In adults, the expression of maltase-glucoamylase and sucrose-isomaltase showed the highest values in the middle intestine, while the liver and anterior and posterior intestine showed low expression levels. Other enzymes showed low expression in all tissues, with the exception of leucine aminopeptidase, which showed high expression in liver. In larvae whole-body samples of D. latifrons, maltase-glucoamylase and sucrose-isomaltase showed the highest expression from 3 to 5 dph, while other enzymes maintained low levels from hatching to 7 dph. The highest expression of disaccharidases such as maltaseglucoamylase and sucrose-isomaltase corresponded to the beginning of exogenous feeding, suggesting that this species exhibits an herbivorous profile. However, the presence of proteolytic enzymes may indicate that D. latifrons is programmed to be able to digest other substrates. This information will contribute to the development of larval feeding protocols to produce chame juveniles in laboratory conditions, as prior larval feeding essays have not been successful, using either live feeds or commercial fish larval diets. K E Y W O R D S chame, digestive enzyme, Dormitator latifrons, gene expression How to cite this article: Morelos-Castro, Román-Reyes JC, Luis-Villaseñor IE, Ramírez-Pérez JS, Rodríguez-Montes de Oca GA. Expression analyses of digestive enzymes during early development and in adults of the chame fish Dormitator latifrons. Aquac Res. 2020;51:265-275. https ://doi.

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“…Knowledge of the biochemical characteristics (e.g., response to pH, temperature and kinetic parameters) of digestive enzymes of prejuveniles in the wild is lacking. The maintenance of the activity of various digestive enzymes in the intestine over a wide range of pH, temperature and Michaelis-Menten kinetics has been described in various fish under controlled conditions (del Valle et al, 2016;Gioda et al, 2017;Huo et al, 2019;Kuz'mina et al, 1996). The tolerance to a wide range of temperatures is one of the characteristics of M. liza that supports its potential use in aquaculture.…”

Section: Discussionmentioning

confidence: 98%

Understanding the early ontogenetic stages of Mugil liza (Mugilidae): Morphological traits and digestive/metabolic profile of pre‐juveniles after recruitment

Albanesi

González‐Castro

López-Mañanes

2020

Journal of Fish Biology

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The family Mugilidae consists mainly of diadromous species, whose reproduction occurs in offshore waters. Pre-juveniles shift their diet in the surf zone (zooplanktophagous to iliophagous). Later, during their recruitment into estuaries, huge changes take place in their digestive system. However, digestive and metabolic characteristics and some morphological traits at recruitment are unknown for Mugilidae. We performed comparative studies on early and late pre-juveniles of Mugil liza recruited in Mar Chiquita Coastal Lagoon (37 32 0-37 45 0 S, 57 19 0-57 26 0 W, Argentina). We determined digestive enzyme activities (intestine), energy reserves (liver/muscle), total/standard length, total weight, intestinal coefficient, hepatosomatic index and retroperitoneal fat. Pre-juveniles exhibited amylase, maltase, sucrase, lipase, trypsin and aminopeptidase-N (APN) activities, which were maintained over a wide range of pH and temperature, and exhibited Michaelis-Menten kinetics. In late pre-juveniles, amylase (422 ± 131 μmol maltose min −1 mgprot −1), sucrase (86 ± 14 mg glucose min −1 mgprot −1), trypsin (84 ± 9 μmoles min −1 mgprot −1) and APN (0.58 ± 0.08 μmoles min −1 mgprot −1) activities were higher (42%, 28%, 35% and 28%, respectively) than in the early stage. Also, the intestinal coefficient was higher in late (3.04) compared to early (2.06) pre-juveniles. Moreover, the liver appeared to be a main site of glycogen and triglyceride storage in late pre-juveniles, muscle being the site of storage in early pre-juveniles, exhibiting higher glycogen, free glucose and protein concentrations (92%, 82%, 32%, respectively). The results suggest that pre-juveniles of M. liza exhibit an adequate digestive battery to perform complete hydrolysis of various dietary substrates, availability of energy reserves and morphological characteristics to support their feeding habit and growth after recruitment. Our results represent an important contribution to knowledge of the ecology and digestive physiology of pre-juveniles of Mugilidae in the wild. K E Y W O R D S digestive enzymes, energy reserves, Mar Chiquita Coastal Lagoon, Mugil liza, pre-juveniles, recruitment Mariano González-Castro and Alejandra López-Mañanes have contributed equally to this study.

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Different feeding habits influence the activity of digestive enzymes in freshwater fish

Cited by 27 publications

References 12 publications

Physiological genomics of dietary adaptation in a marine herbivorous fish

Physiological genomics of dietary adaptation in a marine herbivorous fish

Expression analyses of digestive enzymes during early development and in adults of the chame fishDormitator latifrons

Understanding the early ontogenetic stages of Mugil liza (Mugilidae): Morphological traits and digestive/metabolic profile of pre‐juveniles after recruitment

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