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Potential contributions of gut microbiota to the nutrition of the detritivorous sesarmid crab Parasesarma erythodactyla

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Abstract

Mangrove leaf litter, the dominant food of the detritivorous sesarmid crab Parasesarma erythodactyla, is highly deficient in nitrogen and long-chain polyunsaturated fatty acids. We experimentally investigated potential contributions of the gut microbiota to the nutrition of P. erythodactyla by providing crabs with 13C- and 15N-labelled substrates that could lead to biosynthesis of key amino acids and fatty acids. Antibiotic treatment suppressed the gut microbiota of the crabs by reducing bacteria density to 9 and 52 % of those in the non-treated crabs in the amino acid and fatty acid experiments, respectively. Compound-specific isotopic analysis revealed significant 13C-enrichments in threonine (Thr), isoleucine (Ile), phenylalanine (Phe), and docosahexaenoic acid (DHA) in crabs fed 13C-enriched glucose and palmitic acid, respectively, suggesting that these essential nutrients were de novo synthesized in the crab. Antibiotic treatment affected the incorporation of 13C-label to Thr, suggesting an involvement of the gut microbes in the biosynthesis of this amino acid. On the contrary, levels of 13C-enrichment in Ile, Phe, and DHA in crabs with intact and suppressed gut microbiota were comparable, suggesting that these compounds may be synthesized endogenously by the crab. Differences between crabs with and without an intact gut microbiota, however, may have been undetectable because of the high variability in 13C-enrichment of these compounds and the incomplete removal of gut micro-organisms in the antibiotic-treated crabs. Genetic and biochemical capacities enabling the gut microbes to de novo synthesize Ile, Phe, and DHA, therefore, need to be verified by additional approaches.

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References

  • Abdulkadir S, Tsuchiya M (2008) One-step method for quantitative and qualitative analysis of fatty acids in marine animal samples. J Exp Mar Biol Ecol 354:1–8. doi:10.1016/j.jembe.2007.08.024

    Article  CAS  Google Scholar 

  • Adachi K, Toriyama K, Azekura T, Morioka K, Tongnunui P, Ikejima K (2012) Potent cellulase activity in the hepatopancreas of mangrove crabs. Fish Sci 78:1309–1314. doi:10.1007/s12562-012-0547-8

    Article  CAS  Google Scholar 

  • Akimoto M, Ishii T, Yamagaki K, Ohtaguchi K, Koide K, Yazawa K (1990) Production of eicosapentaenoic acid by a bacterium isolated from mackerel intestines. J Am Oil Chem Soc 67:911–915. doi:10.1007/bf02541846

    Article  CAS  Google Scholar 

  • Allardyce NJ, Linton SM (2012) Synergistic interaction of an endo-beta-1,4-glucanase and a beta-glucohydrolase leads to more efficient hydrolysis of cellulose-like polymers in the gecarcinid land crab, Gecarcoidea natalis. Aust J Zool 60:299–302. doi:10.1071/ZO12074

    Article  Google Scholar 

  • Alongi DM (1994) Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests. Oecologia 98:320–327. doi:10.1007/bf00324220

    Article  Google Scholar 

  • Amin MR, Onodera R (1997) Synthesis of phenylalanine and production of other related compounds from phenylpyruvic acid and phenylacetic acid by ruminal bacteria, protozoa, and their mixture in vitro. J Gen Appl Microbiol 43:9–15. doi:10.2323/jgam.43.9

    Article  CAS  Google Scholar 

  • Armitage ME, Raymont JEG, Morris RJ (1981) Amino-acid synthesis in Neomysis integer and Gnathophausia sp-feeding experiments using C14-labeled precursors. Comp Biochem Physiol B Biochem Mol Biol 68:183–191. doi:10.1016/0305-0491(81)90086-9

    Article  Google Scholar 

  • Bell MV, Dick JR, Kelly MS (2001) Biosynthesis of eicosapentaenoic acid in the sea urchin Psammechinus miliaris. Lipids 36:79–82. doi:10.1007/s11745-001-0671-2

    Article  CAS  Google Scholar 

  • Bender DA (2012) Amino acid metabolism. Wiley-Blackwell, Chichester

    Book  Google Scholar 

  • Blomquist GJ, Borgeson CE, Vundla M (1991) Polyunsaturated fatty-acids and eicosanoids in insects. Insect Biochem 21:99–106. doi:10.1016/0020-1790(91)90069-q

    Article  CAS  Google Scholar 

  • Bosire JO, Dahdouh-Guebas F, Kairo JG, Kazungu J, Dehairs F, Koedam N (2005) Litter degradation and CN dynamics in reforested mangrove plantations at Gazi Bay, Kenya. Biol Conserv 126:287–295. doi:10.1016/j.biocon.2005.06.007

    Article  Google Scholar 

  • Brett M, Müller-Navarra D (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshw Biol 38:483–499. doi:10.1046/j.1365-2427.1997.00220.x

    Article  CAS  Google Scholar 

  • Bui THH, Lee SY (2014) Does ‘you are what you eat’ apply to mangrove grapsid crabs? PLoS ONE 9:e89074. doi:10.1371/journal.pone.0089074

    Article  Google Scholar 

  • Bui THH, Lee SY (2015) Endogenous cellulase production in the leaf litter foraging mangrove crab Parasesarma erythodactyla. Comp Biochem Physiol B 179:27–36. doi:10.1016/j.cbpb.2014.09.004

    Article  CAS  Google Scholar 

  • Buzzi M, Henderson RJ, Sargent JR (1996) The desaturation and elongation of linolenic acid and eicosapentaenoic acid by hepatocytes and liver microsomes from rainbow trout (Oncorhynchus mykiss) fed diets containing fish oil or olive oil. Biochim Biophys Acta Lipids Lipid Metabol 1299:235–244. doi:10.1016/0005-2760(95)00211-1

    Article  Google Scholar 

  • Camilleri JC (1992) Leaf-litter processing by invertebrates in a mangrove forest in Queensland. Mar Biol 114:139–145. doi:10.1007/BF00350863

    Google Scholar 

  • Clark JH, Klusmeyer TH, Cameron MR (1992) Microbial protein-synthesis and flows of nitrogen fractions to the duodenum of dairy-cows. J Dairy Sci 75:2304–2323. doi:10.3168/jds.S0022-0302(92)77992-2

    Article  CAS  Google Scholar 

  • Cook HW, McMaster CR (2002) Fatty acid desaturation and chain elongation in eukaryotes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes, 4th edn. Elsevier, Amsterdam, pp 181–204

    Chapter  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. doi:10.1146/annurev.arplant.48.1.355

    Article  CAS  Google Scholar 

  • de Carvalho LPS, Argyrou A, Blanchard JS (2005) Slow-onset feedback inhibition: inhibition of Mycobacterium tuberculosis α-isopropylmalate synthase by l-Leucine. J Am Chem Soc 127:10004–10005. doi:10.1021/ja052513h

    Article  Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92. doi:10.1146/annurev.ento.49.061802.123416

    Article  CAS  Google Scholar 

  • Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37. doi:10.1146/annurev.ento.43.1.17

    Article  CAS  Google Scholar 

  • Duggleby RG, Pang SS (2000) Acetohydroxyacid synthase. J Bioc Mol Biol 33:1–36

    CAS  Google Scholar 

  • Fong W, Mann KH (1980) Role of gut flora in the transfer of amino-acids through a marine food-chain. Can J Fish Aquat Sci 37:88–96. doi:10.1139/f80-009

    Article  Google Scholar 

  • Gellerman JL, Schlenk H (1979) Methyl-directed desaturation of arachidonic to eicosapentaenoic acid in the fungus, Saprolegnia parasitica. Biochim Biophys Acta Lipids Lipid Metabol 573:23–30. doi:10.1016/0005-2760(79)90169-3

    Article  CAS  Google Scholar 

  • Gulmann LK (2004) Gut-associated microbial symbionts of the marsh fiddler crab, Uca pugnax. Ph.D. thesis. Massachusetts Institute of Technology, Cambridge

  • Hall D, Lee SY, Meziane T (2006) Fatty acids as trophic tracers in an experimental estuarine food chain: tracer transfer. J Exp Mar Biol Ecol 336:42–53. doi:10.1016/j.jembe.2006.04.004

    Article  CAS  Google Scholar 

  • Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates—a synthesis. Microb Ecol 25:195–231. doi:10.1007/BF00171889

    Article  CAS  Google Scholar 

  • Harris JM, Seiderer LJ, Lucas MI (1991) Gut microflora of two saltmarsh detritivore thalassinid prawns, Upogebia africana and Callianassa kraussi. Microb Ecol 21:277–296. doi:10.1007/BF02539159

    Article  CAS  Google Scholar 

  • Jennerjahn TC, Ittekkot V (2002) Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften 89:23–30. doi:10.1007/s00114-001-0283-x

    Article  Google Scholar 

  • Jeremy MB, Tymoczko JL, Stryer L (2006) Biochemistry. W.H. Freeman, New York

    Google Scholar 

  • Johnston D, Freeman J (2005) Dietary preference and digestive enzyme activities as indicators of trophic resource utilization by six species of crab. Biol Bull 208:36–46. doi:10.2307/3593099

    Article  CAS  Google Scholar 

  • Jøstensen JP, Landfald B (1997) High prevalence of polyunsaturated-fatty-acid producing bacteria in arctic invertebrates. FEMS Microbiol Lett 151:95–101. doi:10.1111/j.1574-6968.1997.tb10400.x

    Article  Google Scholar 

  • Kanazawa A, Teshima SI, Ono K (1979) Relationship between essential fatty acid requirements of aquatic animals and the capacity for bioconversion of linolenic acid to highly unsaturated fatty acids. Comp Biochem Physiol B Biochem Mol Biol 63:295–298

    Article  CAS  Google Scholar 

  • Kohlhaw GB (2003) Leucine biosynthesis in fungi: entering metabolism through the back door. Microbiol Mol Biol Rev 67:1–15. doi:10.1128/MMBR.67.1.1-15.2003

    Article  CAS  Google Scholar 

  • Kunau WH, Dommes V, Schulz H (1995) β-Oxidation of fatty acids in mitochondria, peroxisomes, and bacteria: a century of continued progress. Prog Lipid Res 34:267–342. doi:10.1016/0163-7827(95)00011-9

    Article  CAS  Google Scholar 

  • Kwok PW, Lee SY (1995) Growth performance of two mangrove sesarmid crabs, Chiromanthes bidens and Parasesarma affinis under different diets. Hydrobiologia 295:141–148. doi:10.1007/BF00029121

    Article  Google Scholar 

  • Larsen T, Ventura M, O’Brien DM, Magid J, Lomstein BA, Larsen J (2011) Contrasting effects of nitrogen limitation and amino acid imbalance on carbon and nitrogen turnover in three species of Collembola. Soil Biol Biochem 43:749–759. doi:10.1016/j.soilbio.2010.12.008

    Article  CAS  Google Scholar 

  • Lauritzen L, Hansen HS, Jorgensen MH, Michaelsen KF (2001) The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res 40:1–94. doi:10.1016/s0163-7827(00)00017-5

    Article  CAS  Google Scholar 

  • Lee SY (1990) Primary productivity and particulate organic-matter flow in an estuarine mangrove wetland in Hong Kong. Mar Biol 106:453–463. doi:10.1007/bf01344326

    Article  Google Scholar 

  • Linton SM, Greenaway P (2007) A review of feeding and nutrition of herbivorous land crabs: adaptations to low quality plant diets. J Comp Physiol B 177:269–286. doi:10.1007/s00360-006-0138-z

    Article  Google Scholar 

  • Linton SM, Shirley AJ (2011) Isozymes from the herbivorous gecarcinid land crab, Gecarcoidea natalis that possess both lichenase and endo-beta-1,4-glucanase activity. Comp Biochem Physiol B 160:44–53. doi:10.1016/j.cbpb.2011.05.007

    Article  CAS  Google Scholar 

  • Lunau M, Lemke A, Walther K, Martens-Habbena W, Simon M (2005) An improved method for counting bacteria from sediments and turbid environments by epifluorescence microscopy. Environ Microbiol 7:961–968. doi:10.1111/j.1462-2920.2005.00767.x

    Article  Google Scholar 

  • Maeda H, Dudareva N (2012) The Shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol 63:73–105. doi:10.1146/annurev-arplant-042811-105439

    Article  CAS  Google Scholar 

  • Malley DF (1978) Degradation of mangrove leaf litter by tropical sesarmid crab Chiromanthes onychophorum. Mar Biol 49:377–386. doi:10.1007/BF00455032

    Article  Google Scholar 

  • McConn M, Browse J (1998) Polyunsaturated membranes are required for photosynthetic competence in a mutant of Arabidopsis. Plant J 15:521–530. doi:10.1046/j.1365-313X.1998.00229.x

    Article  CAS  Google Scholar 

  • Metges CC (2000) Contribution of microbial amino acids to amino acid homeostasis of the host. J Nutr 130:1857S–1864S

    CAS  Google Scholar 

  • Metz JG, Roessler P, Facciotti D, Levering C, Dittrich F, Lassner M, Valentine R, Lardizabal K, Domergue F, Yamada A, Yazawa K, Knauf V, Browse J (2001) Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293:290–293. doi:10.1126/science.1059593

    Article  CAS  Google Scholar 

  • Mfilinge PL, Meziane T, Bachok Z, Tsuchiya M (2003) Fatty acids in decomposing mangrove leaves: microbial activity, decay and nutritional quality. Mar Ecol Prog Ser 265:97–105. doi:10.3354/meps265097

    Article  CAS  Google Scholar 

  • Mohammed N, Onodera R, Khan RI (1999) Tryptophan biosynthesis and production of other related compounds from indolepyruvic acid by mixed ruminal bacteria, protozoa, and their mixture in vitro. J Gen Appl Microbiol 45:143–147. doi:10.2323/jgam.45.143

    Article  CAS  Google Scholar 

  • Mourente G, Tocher DR (1994) In-vivo metabolism of [1-14C]linolenic acid (18:3(n-3)) and [1-14C]eicosapentaenoic acid (20:5(n-3)) in a marine fish: time-course of the desaturation/elongation pathway. Biochim Biophys Acta Lipids Lipid Metabol 1212:109–118. doi:10.1016/0005-2760(94)90195-3

    Article  CAS  Google Scholar 

  • Newsome SD, Fogel ML, Kelly L, del Rio CM (2011) Contributions of direct incorporation from diet and microbial amino acids to protein synthesis in Nile tilapia. Funct Ecol 25:1051–1062. doi:10.1111/j.1365-2435.2011.01866.x

    Article  Google Scholar 

  • Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113–118. doi:10.3354/ame014113

    Article  Google Scholar 

  • Owen JM, Adron JW, Middleton C, Cowey CB (1975) Elongation and desaturation of dietary fatty acids in turbot Scophthalmus maximus L, and rainbow-trout, Salmo gairdnerii rich. Lipids 10:528–531. doi:10.1007/bf02532354

    Article  CAS  Google Scholar 

  • Park JH, Lee SY (2010) Metabolic pathways and fermentative production of l-aspartate family amino acids. Biotechnol J 5:560–577. doi:10.1002/biot.201000032

    Article  CAS  Google Scholar 

  • Pinn EH, Rogerson A, Atkinson RJA (1997) Microbial flora associated with the digestive system of Upogebia stellata (Crustacea: Decapoda: Thalassinidea). J Mar Biol Assoc UK 77:1083–1096. doi:10.1017/S0025315400038649

    Article  Google Scholar 

  • Poovachiranon S, Tantichodok P (1991) The role of sesarmid crabs in the mineralisation of leaf litter of Rhizophora apiculata in a mangrove, southern Thailand. Phuket Mar Biol Cent Res Bull 56:63–74

    Google Scholar 

  • Pruitt NL (1990) Adaptations to temperature in the cellular membranes of crustacea membrane structure and metabolism. J Therm Biol 15:1–8. doi:10.1016/0306-4565(90)90040-o

    Article  Google Scholar 

  • Robertson AI (1988) Decomposition of mangrove leaf litter in tropical Australia. J Exp Mar Biol Ecol 116:235–247. doi:10.1016/0022-0981(88)90029-9

    Article  Google Scholar 

  • Russell-Hunter WD (1970) Aquatic productivity: an introduction to some basic aspects of biological oceanography and limnology. Ollier-Macmillan, London

    Google Scholar 

  • Salunkhe D, Tiwari N, Walujkar S, Bhadekar R (2011) Halomonas sp nov., an EPA-producing mesophilic marine isolate from the Indian Ocean. Pol J Microbiol 60:73–78

    CAS  Google Scholar 

  • Shulse CN, Allen EE (2011) Diversity and distribution of microbial long-chain fatty acid biosynthetic genes in the marine environment. Environ Microbiol 13:684–695. doi:10.1111/j.1462-2920.2010.02373.x

    Article  CAS  Google Scholar 

  • Skov MW, Hartnoll RG (2002) Paradoxical selective feeding on a low-nutrient diet: Why do mangrove crabs eat leaves? Oecologia 131:1–7. doi:10.1007/s00442-001-0847-7

    Article  Google Scholar 

  • Stanley-Samuelson DW (1994) Assessing the significance of prostaglandins and other eicosanoids in insect physiology. J Insect Physiol 40:3–11. doi:10.1016/0022-1910(94)90106-6

    Article  CAS  Google Scholar 

  • Tayasu I, Sugimoto A, Wada E, Abe T (1994) Xylophagous termites depending on atmospheric nitrogen. Naturwisenschaften 81:229–231

    Article  Google Scholar 

  • Thongtham N, Kristensen E (2005) Carbon and nitrogen balance of leaf-eating sesarmid crabs (Neoepisesarma versicolor) offered different food sources. Estuar Coast Shelf Sci 65:213–222. doi:10.1016/j.ecss.2005.05.014

    Article  Google Scholar 

  • Tremblay L, Benner R (2006) Microbial contributions to N-immobilization and organic matter preservation in decaying plant detritus. Geochim Cosmochim Acta 70:133–146. doi:10.1016/j.gca.2005.08.024

    Article  CAS  Google Scholar 

  • Vagner M, Santigosa E (2011) Characterization and modulation of gene expression and enzymatic activity of delta-6 desaturase in teleosts: a review. Aquaculture 315:131–143. doi:10.1016/j.aquaculture.2010.11.031

    Article  CAS  Google Scholar 

  • Werry J, Lee SY (2005) Grapsid crabs mediate link between mangrove litter production and estuarine planktonic food chains. Mar Ecol Prog Ser 293:165–176. doi:10.3354/meps293165

    Article  Google Scholar 

  • Xu W, Mai KS, Ai QH, Tan BP, Zhang WB, Ma HM, Liufu ZG (2011) Influence of 18:2n-6/20:5n-3 ration in diets on growth and fatty acid composition of juvenile abalone, Haliotis discus hannai Ino. Aquac Nutr 17:346–351. doi:10.1111/j.1365-2095.2010.00802.x

    Article  CAS  Google Scholar 

  • Yano Y, Nakayama A, Yoshida K (1997) Distribution of polyunsaturated fatty acids in bacteria present in intestines of deep-sea fish and shallow-sea poikilothermic animals. Appl Environ Microbiol 63:2572–2577

    CAS  Google Scholar 

  • Zieman JC, Macko SA, Mills AL (1984) Role of seagrasses and mangroves in estuarine food webs—temporal and spatial changes in stable isotope composition and amino-acid content during decomposition. Bull Mar Sci 35:380–392

    Google Scholar 

  • Zimmer M, Bartholme S (2003) Bacterial endosymbionts in Asellus aquaticus (Isopoda) and Gammarus pulex (Amphipoda) and their contribution to digestion. Limnol Oceanogr 48:2208–2213. doi:10.4319/lo.2003.48.6.2208

    Article  Google Scholar 

  • Zimmer M, Danko JP, Pennings SC, Danford AR, Ziegler A, Uglow RF, Carefoot TH (2001) Hepatopancreatic endosymbionts in coastal isopods (Crustacea : Isopoda), and their contribution to digestion. Mar Biol 138:955–963. doi:10.1007/s002270000519

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Helen Stratton (Smart Water Research Centre, Griffith University) for helping with the quantification of the gut micro-organisms. T.H.H.B. was supported by an Australia Endeavour Postgraduate Award.

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Correspondence to Shing Yip Lee.

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Bui, T.H.H., Lee, S.Y. Potential contributions of gut microbiota to the nutrition of the detritivorous sesarmid crab Parasesarma erythodactyla . Mar Biol 162, 1969–1981 (2015). https://doi.org/10.1007/s00227-015-2723-8

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