Acid lysis of macroalgae by marine herbivorous fishes: myth or digestive mechanism?

Zemke‐White, W. Lindsey; Clements, Kendall D.; Harris, Philip J.

doi:10.1016/s0022-0981(98)00124-5

Cited by 30 publications

(23 citation statements)

References 28 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Among the factors which could have limited these processes are redox, pH, sulfate concentration, and gut throughput time. However, low redox levels which would be conducive to methanogenesis have been reported in several species closely related to those in this study (13), and with the possible exception of O. pullus the gut pH of these species (50) would be unlikely to preclude the growth of methanogens. Levels of sulfate in the gastrointestinal tract (Ն20 mM) are unlikely to be limiting to sulfate reduction, as rates much higher than those reported here have been achieved in other anaerobic environments at much lower levels of the acceptor and at similar temperatures (31,32,49).…”

Section: Discussionmentioning

confidence: 45%

Hindgut Fermentation in Three Species of Marine Herbivorous Fish

Mountfort

Campbell

Clements

2002

Appl Environ Microbiol

157

156

View full text Add to dashboard Cite

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 ...

show abstract

Section: Discussionmentioning

confidence: 45%

Hindgut Fermentation in Three Species of Marine Herbivorous Fish

Mountfort

Campbell

Clements

2002

Appl Environ Microbiol

157

156

View full text Add to dashboard Cite

show abstract

“…However, most algae have refractory cell walls (Zemke-White et al 1999;2000), and their nitrogen content is lower than that in the tissues of herbivores (Menzel 1959;Mattson 1980). On coral reefs, some herbivorous fishes compensate for this algal indigestibility and the shortage of nitrogen by defending territories that consist of abundant filamentous algae.…”

Section: Introductionmentioning

confidence: 99%

“…Territorial damselfishes defend their territories against intruding herbivores and manage farms of filamentous algae as their exclusive feeding sites (Ceccarelli et al 2001;Jones et al 2006). In farms, territorial damselfishes browse mainly on the upright axes of filamentous algae (Hiatt and Strasburg 1960;Hata and Kato 2002), and lyse the cell membranes of these algae through refractory cell walls in highly acidic stomachs for subsequent digestion of cell contents by fish enzymes (Zemke-White et al 1999;2000), and absorb them in the long intestines (Horn 1989;Cleveland and Montgomery 2003). Additionally, some of these damselfishes are known to ingest detritus (Wilson and Bellwood 1997;Wilson et al 2003) and/or benthic animals living in the farms (Lobel 1980;Robertson and Polunin 1981;Zeller 1988) to increase nitrogen intake.…”

Section: Introductionmentioning

confidence: 99%

Food habits of the farmer damselfishStegastes nigricansinferred by stomach content, stable isotope, and fatty acid composition analyses

Hata

Umezawa

2011

Ecological Research

View full text Add to dashboard Cite

This content has not been published or submitted for publication elsewhere in any language, and all authors have contributed significantly, and are in agreement with the content of the manuscript. 2 AbstractThe territorial damselfish, Stegastes nigricans, maintains algal farms by excluding invading herbivores and weeding unpalatable algae from its territories. In Okinawa, Japan, S. nigricans farms are exclusively dominated by Polysiphonia sp., a highly digestible filamentous rhodophyte. This study was aimed at determining the diet of S.nigricans in Okinawa and its dependency on these almost-monoculture algal farms based on stomach contents and chemical analyses. Stomach content analyses revealed that all available food items in the algal farms (i.e., algae, benthic animal inhabitants, trapped detritus) were contained in fish stomachs, but amorphous organic matter accounted for 68% of the contents. Therefore, carbon and nitrogen stable isotope ratios and fatty acid (FA) compositions were analyzed to trace items actually assimilated in their bodies. Stable isotope analyses showed that benthic animals were an important food source even for this farmer fish. Two essential FAs (EFA), 20:4n6 and 20:5n3, which are produced only by rhodophytes among available food items, were rich in the muscle tissue of S. nigricans as well as in algal mats and detritus, suggesting that algal mats contribute EFAs to S. nigricans directly and indirectly through the food web. In conclusion, S. nigricans ingested algal mats, detritus and benthic animals maintained within its farm. Algae and detritus were original sources of EFAs, and benthic animals, which were much more abundant in the farms than in outside territories, provided a nitrogen-rich dietary source for the fish.

show abstract

“…These observations suggest a niche where cellobioase activity may be important for V. fischeri. Many herbivorous fish partially digest cellulose by acid hydrolysis in their stomachs (74), and it is believed that bacterial cellulases contribute to the digestion of the cellulose in the gut, as with termites and ruminants (47,70). Although V. fischeri does not contain a cellulase, it is possible that either the acidity of the fish's stomach or other bacteria in a fish's intestine could break down cellulose into cellobiose, allowing V. fischeri to consume it.…”

Section: Discussionmentioning

confidence: 99%

Identification of a Cellobiose Utilization Gene Cluster with Cryptic β-Galactosidase Activity in Vibrio fischeri

Adin

Visick

Stabb

2008

Appl Environ Microbiol

View full text Add to dashboard Cite

Cellobiose utilization is a variable trait that is often used to differentiate members of the family Vibrionaceae. We investigated how Vibrio fischeri ES114 utilizes cellobiose and found a cluster of genes required for growth on this ␤-1,4-linked glucose disaccharide. This cluster includes genes annotated as a phosphotransferase system II (celA, celB, and celC), a glucokinase (celK), and a glucosidase (celG). Directly downstream of celCBGKA is celI, which encodes a LacI family regulator that represses cel transcription in the absence of cellobiose. When the celCBGKAI gene cluster was transferred to cellobiose-negative strains of Vibrio and Photobacterium, the cluster conferred the ability to utilize cellobiose. Genomic analyses of naturally cellobiosepositive Vibrio species revealed that V. salmonicida has a homolog of the celCBGKAI cluster, but V. vulnificus does not. Moreover, bioinformatic analyses revealed that CelG and CelK share the greatest homology with glucosidases and glucokinases in the phylum Firmicutes. These observations suggest that distinct genes for cellobiose utilization have been acquired by different lineages within the family Vibrionaceae. In addition, the loss of the celI regulator, but not the structural genes, attenuated the ability of V. fischeri to compete for colonization of its natural host, Euprymna scolopes, suggesting that repression of the cel gene cluster is important in this symbiosis. Finally, we show that the V. fischeri cellobioase (CelG) preferentially cleaves ␤-D-glucose linkages but also cleaves ␤-D-galactose-linked substrates such as 5-bromo-4-chloro-3-indolyl-␤-D-galactoside (X-gal), a finding that has important implications for the use of lacZ as a marker or reporter gene in V. fischeri.

show abstract

Acid lysis of macroalgae by marine herbivorous fishes: myth or digestive mechanism?

Cited by 30 publications

References 28 publications

Hindgut Fermentation in Three Species of Marine Herbivorous Fish

Hindgut Fermentation in Three Species of Marine Herbivorous Fish

Food habits of the farmer damselfishStegastes nigricansinferred by stomach content, stable isotope, and fatty acid composition analyses

Identification of a Cellobiose Utilization Gene Cluster with Cryptic β-Galactosidase Activity in Vibrio fischeri

Contact Info

Product

Resources

About