Skip to main content
Log in

Bacterial ectosymbionts colonizing gills of two Caribbean mangrove crabs

  • Short Communications
  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

We describe here the interactions between bacterial ectosymbionts and two Caribbean mangrove crabs: Aratus pisonii (Sesarmidae) and Minuca rapax (Ocypodidae). Specimens of A. pisonii and M. rapax were collected in Guadeloupe from mangrove trees (Rhizophora mangle) and from the mangrove mud, respectively. Ectosymbionts colonizing gills in all host individuals were observed using scanning and transmission electron microscopy (SEM and TEM). No intracellular bacteria were observed in gills cells suggesting that the biofilm only occurs on the surface of the gills. For A. pisonii and M. rapax, four different bacterial morphotypes were distributed throughout the surface of gill lamellae. Different sizes and lengths were observed in the bacterial population colonizing A. pisonii and M. rapax. Either symbionts cover the entire surface of the gills, or they formed irregularly distributed patches. Molecular analyses (high-throughput amplicon sequencing of bacterial 16S rRNA-encoding genes) confirmed the occurrence of multiple bacterial taxonomic units, with dominance of Alphaproteobacteria and Bacteroidetes in both host species. However, dominant bacterial phylotypes were not shared between A. pisonii and M. rapax. This suggests that each species of these semiterrestrial crabs may harbor a specific and distinct bacterial community despite living in the same mangroves. The discussion compares the bacterial compositions of the two species and their potential functions are hypothesized. Further investigations are needed to confirm the specificity and nature of the symbiosis, including potential exchanges occurring between the partners.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Availability of data and material

All data are available on GenBank NCBI.

Code availability

Not applicable.

References

  • Abouna S, Gonzalez-Rizzo S, Grimonprez A, Gros O (2015) First description of Sulphur-oxidizing bacterial symbiosis in a cnidarian (Medusozoa) living in sulphidic shallow-water environments. PLoS One 10:e0127625

    Article  Google Scholar 

  • Amir A, McDonald D, Navas-Molina JA, Kopylova E, Morton JT, Zech Xu Z, Kightley EP, Thompson LR, Hyde ER, Gonzalez A, Knight R (2017) Deblur rapidly resolves singlenucleotide community sequence patterns. mSystems 2:e00191–16

  • Booth J (2018) Ecology of the Mangrove Microbiome (Doctoral dissertation)

  • Booth JM, Fusi M, Marasco R, Mbobo T, Daffonchio D (2019) Fiddler crab bioturbation determines consistent changes in bacterial communities across contrasting environmental conditions. Sci Rep 9:3749

    Article  Google Scholar 

  • Brissac T, Merçot H, Gros O (2011) Lucinidae/sulfur-oxidizing bacteria: ancestral heritage or opportunistic association? Further insights from the Bohol Sea (the Philippines). FEMS Microbiol Ecol 75:63–76

    Article  CAS  Google Scholar 

  • Callahan BJ, McMurdie PJ, Holmes SP (2017) Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J 11:2639–2643

    Article  Google Scholar 

  • Christy JH (1978) Adaptive significance of reproductive cycles in the fiddler crab Uca pugilator: a hypothesis. Science 199:453–455

    Article  CAS  Google Scholar 

  • Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66:1692–1697

    Article  CAS  Google Scholar 

  • Distel D (2003) The biology of marine wood boring bivalves and their bacterial endosymbionts. ACS Symp Ser 845:253–271

    Article  CAS  Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740

    Article  CAS  Google Scholar 

  • Duperron S, Halary S, Habiballah M, Gallet A, Huet H, Duval C, Bernard C, Marie B (2019) Response of fish gut microbiota to toxin-containing cyanobacterial extracts: a microcosm study on the medaka (Oryzias latipes). Environ Sci Technol Lett 6:341–347

    Article  CAS  Google Scholar 

  • Duperron S, Laurent MCZ, Gaill F, Gros O (2008) Sulphur-oxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls. FEMS Microbiol Ecol 63:338–349

    Article  CAS  Google Scholar 

  • Duperron S, Pottier M-A, Léger N, Gaudron SM, Puillandre N, le Prieur S, Sigwart JD, Ravaux J, Zbinden M (2013) A tale of two chitons: is habitat specialisation linked to distinct associated bacterial communities? FEMS Microbiol Ecol 83:552–567

    Article  CAS  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  Google Scholar 

  • Fisher CR, Childress JJ (1986) Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi. Mar Biol 93:59–68

    Article  CAS  Google Scholar 

  • Frenkiel L, Gros O, Mouëza M (1996) Gill structure in Lucina pectinata (Bivalvia: Lucinidae) with reference to hemoglobin in bivalves with symbiotic sulphur-oxidizing bacteria. Mar Biol 125:511–524

  • Goffredi SK, Jones WJ, Erhlich H, Springer A, Vrijenhoek RC (2008) Epibiotic bacteria associated with the recently discovered yeti crab, Kiwa hirsuta. Environ Microbiol 10:2623–2634

    Article  CAS  Google Scholar 

  • Goffredi SK, Waren A, Orphan VJ et al (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl Environ Microbiol 70:3082–3090

    Article  CAS  Google Scholar 

  • Gros O, Gaill F (2007) Extracellular bacterial association in gills of “wood mussels”. Cah Biol Mar 48:103

  • Hall M, Beiko RG (2018) 16S rRNA gene analysis with QIIME2. Methods Mol Biol 1849:113–129

    Article  CAS  Google Scholar 

  • Himmel D, Maurin LC, Gros O, Mansot J-L (2009) Raman microspectrometry sulfur detection and characterization in the marine ectosymbiotic nematode Eubostrichus dianae (Desmodoridae, Stilbonematidae). Mol Biol Cell 101:43–54

    CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Lefort V, Longueville J-E, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424

    Article  CAS  Google Scholar 

  • Liang J-B, Chen Y-Q, Lan C-Y, Tam NFY, Zan QJ, Huang LN (2007) Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 150:739–747

    Article  Google Scholar 

  • Li K, Guan W, Wei G, Liu B, Xu J, Zhao L, Zhang Y (2007) Phylogenetic analysis of intestinal bacteria in the Chinese mitten crab (Eriocheir sinensis). J Appl Microbiol 103:675–682

    Article  CAS  Google Scholar 

  • Li X, Liu Y, Chen Z, Liu LZ, Liu ZP, Liu Y (2016) Membranicola marinus gen. Nov., sp. nov., a new member of the family Saprospiraceae isolated from a biofilter in a recirculating aquaculture system. Int J Syst Evol Microbiol 66:1275–1280

    Article  CAS  Google Scholar 

  • Milne Edwards H (1837) Histoire naturelle des crustacés. L’Institute, Paris 5:225

  • Nyholm SV, McFall-Ngai M (2004) The winnowing: establishing the squid–vibrio symbiosis. Nat Rev Microbiol 2:632–642

    Article  CAS  Google Scholar 

  • Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414

    Article  CAS  Google Scholar 

  • Rützler K, Feller C (1988) Mangrove swamp communities. Oceanus 30:10

    Google Scholar 

  • Sharma S, Shukla KP, Singh V, Singh J, Devi S, Tewari A (2013) Plant–microbe Symbiosis: perspectives and applications. In: Arora NK (ed) plant microbe symbiosis: fundamentals and advances. Springer India, pp 119–145

    Chapter  Google Scholar 

  • Smith SI (1870) III. Notes on American Crustacea. No. 1. Ocypodidea. Trans Conn Acad 2:113–176

  • Tsuchida S, Suzuki Y, Fujiwara Y, Kawato M, Uematsu K, Yamanaka T, Mizota C, Yamamoto H (2011) Epibiotic association between filamentous bacteria and the vent-associated galatheid crab, Shinkaia crosnieri (Decapoda: Anomura). J Mar Biolog Assoc UK 91:23–32

    Article  CAS  Google Scholar 

  • Warner GF (1967) The life history of the mangrove tree crab Aratus pisonii. J Zool 153:321–335

  • Zbinden M, Le Bris N, Gaill F, Compere P (2004) Distribution of bacteria and associated minerals in the gill chamber of the vent shrimp Rimicaris exoculata and related biogeochemical processes. Mar Ecol Prog Ser 284:237–251

    Article  Google Scholar 

  • Zbinden M, Pailleret M, Ravaux J, Gaudron SM, Hoyoux C, Lambourdière J, Warén A, Lorion J, Halary S, Duperron S (2010) Bacterial communities associated with the wood-feeding gastropod Pectinodonta sp. (Patellogastropoda, Mollusca). FEMS Microbiol Ecol 74:450–463

    Article  CAS  Google Scholar 

  • Zhang M, Sun Y, Chen L, Cai C, Qiao F, du Z, Li E (2016) Symbiotic bacteria in gills and guts of chinese mitten crab (Eriocheir sinensis) differ from the free-living bacteria in water. PLoS One 11:e0148135

Download references

Funding

N. Beziat was supported by a grant from “Conseil Régional de la Guadeloupe” and by Caribaea Initiative. We acknowledge the financial support of the CNRS MITI X-Life 2018–2019 program (CABMAN project) for the sequencing.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization and supervision: O.G (Olivier Gros) and S.D. (Sébastien Duperron), Phylogenetic studies: S.D. (Sébastien Duperron) and S.H (Sébastien Halary). Ultrastructural studies: N.B. (Naëma Béziat) and O.G. Collection of specimens and preparation for ultrastructural studies: N.B. and C.A. (Catherine Azède).

All the authors contributed to the writing and editing the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Naëma S. Béziat.

Ethics declarations

Conflicts of interest/competing interests

There is no conflicts of interest or competing interests.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Béziat, N.S., Duperron, S., Halary, S. et al. Bacterial ectosymbionts colonizing gills of two Caribbean mangrove crabs. Symbiosis 85, 105–114 (2021). https://doi.org/10.1007/s13199-021-00801-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-021-00801-4

Keywords

Navigation