Hindgut Fermentation in Three Species of Marine Herbivorous Fish

Abstract

Symbioses with gut microorganisms provides a means by which terrestrial herbivores are able to obtain energy. These microorganisms ferment cell wall materials of plants to short-chain fatty acids (SCFA), which are then absorbed and used by the host animal. Many marine herbivorous fishes contain SCFA (predominantly acetate) in their hindgut, indicative of gut microbial activity, but rates of SCFA production have not been measured. Such information is an important prerequisite to understanding the contribution that gut microorganisms make in satisfying the energy needs of the fish. We have estimated the rates of acetate production in the gut of three species of temperate marine herbivorous fish from northeastern New Zealand: Kyphosus sydneyanus (family Kyphosidae), Odax pullus (family Odacidae), and Aplodactylus arctidens (family Aplodactylidae). Ex vivo preparations of freshly caught fish were maintained with their respiratory and circulatory systems intact, radiolabeled acetate was injected into ligated hindgut sections, and gut fluid was sampled at 20-min intervals for 2 h. Ranges for acetate turnover in the hindguts of the studied species were determined from the slope of plots as the log of the specific radioactivity of acetate versus time and pool size, expressed on a nanomole per milliliter per minute basis. Values were 450 to 570 (K. sydneyanus), 373 to 551 (O. pullus), and 130 to 312 (A. arctidens). These rates are comparable to those found in the guts of herbivorous reptiles and mammals. To determine the contribution of metabolic pathways to the fate of acetate, rates of sulfate reduction and methanogenesis were measured in the fore-, mid-, and hindgut sections of the three fish species. Both rates increased from the distal to proximal end of the hindgut, where sulfate reduction accounted for only a small proportion (<5%) of acetate methyl group transformed to CO 2 , and exceeded methanogenesis from acetate by >50-fold. When gut size was taken into account, acetate uptake from the hindgut of the fish species, determined on a millimole per day per kilogram of body weight basis, was 70 (K. sydneyanus), 18 (O. pullus), and 10 (A. arctidens).Marine herbivorous fish harbor a great diversity of gut microorganisms (1, 9-11, 15, 23, 33, 40, 43, 45). Despite their importance in terms of microbial biodiversity, the role of these microorganisms in the digestive processes of the host fish is not well understood. In contrast, it is well known that most terrestrial vertebrate herbivores contain populations of symbiotic organisms that play a key role in digestion by breaking down plant cell walls (cellulose and hemicellulose) to simple compounds such as short-chain fatty acids (SCFA). The SCFA are then taken up by the host and are used for energy generation and biosynthesis (44).The algae eaten by marine herbivorous fishes are phylogenetically diverse. Unlike terrestrial plants, algae are supported by water and have a lower proportion of structural elements to cell contents (8). Consequently, it is not surprising that ...

Isolation and identification of spoilage causing microorganisms in an Indian mackerel fish (Rastrelliger kanagurta)

“…Molecular genetic techniques offer the ability to identify and delineate fish stock structure where it may not be apparent from phenotypic or behavioural characteristics (Storm and Ringo, 2013). Such techniques have been used successfully to understand the structure of marine fish species (Mountfort et al, 2002;Nelson et al, 2003;Ismail et al, 2008;Jageethadevi et al, 2012).…”

Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies

“…Fish were among the earliest jawed vertebrates to evolve many adaptive immune features that are hallmarks of mammalian systems (Flajnik and Du Pasquier, 2004) and, thus, the known interplay between immunity and mammalian gut bacteria (Hooper et al, 2012) suggests the potential for similar symbioses in rayfinned fish. Fish gut bacteria are generally related to animal-associated microbes, and marine herbivorous fish harbor communities that resemble those of other vertebrates, including gut-fermenting mammals (Mountfort et al, 2002;Sullam et al, 2012). Although community composition across fish species shows correlations with habitat salinity and feeding ecology (Ringø and Strøm, 1994;Ringø and Olsen, 1999;Sullam et al, 2012), a small number of recent surveys have provided glimpses into intraspecific variation in fish gut bacteria and have indicated that there are differences across more distantly related individuals and sampling locations and a sex-dependent effect of diet on gut microbiota (Wilson et al, 2008;Roeselers et al, 2011;Navarrete et al, 2012;Bolnick et al, 2014b).…”

Age, movements, and feeding ecology of northwest Atlantic white sharks estimated from ecogeochemical profiles in vertebrae

“…It is becoming clear that non-ruminant consumers may also rely on microbial gut contributions under certain conditions. More research into the role of the gut microbial community in consumer amino acid metabolism is warranted, particularly for species such as sea turtles, dugongs and herbivorous fishes that are known to have extensive gut microbe communities (e.g., Mountfort et al 2002, Andre et al 2005.…”