Journal of Sea Research 43 (2000) 83–91 www.elsevier.nl/locate/seares
Short Communication
Iron-encrusted diatoms and bacteria epibiotic on Hydrobia ulvae (Gastropoda: Prosobranchia) D.C. Gillan a,*, G.C. Cade´e b a
Laboratoire de Biologie marine, CP 160/15, Universite´ Libre de Bruxelles, 50 av. F. D. Roosevelt, B-1050 Brussels, Belgium b Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands Received 12 July 1999; accepted 12 November 1999
Abstract Rust-coloured shells of the gastropod Hydrobia ulvae collected in the Wadden Sea near Texel and in the Jade Busen were analysed under the scanning electron microscope. Most of the shells were found to be covered with a microbial community encrusted with an iron-rich mineral containing traces of Mn, Mg, Ca and Si (EDAX analysis). The community formed a biofilm including two morphotypes of diatoms identified as Cocconeis placentula and Achnanthes lemmermanni, two morphotypes of slender filamentous bacteria resembling Leucothrix and Flexibacter, aggregates of coccoid cells and large trichomes resembling members of the cyanobacterial orders Pleurocapsales and Stigonematales, respectively. The most frequent microorganisms of the biofilm were diatoms and filamentous bacteria. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Hydrobia; epibiosis; biofilm; diatom; filamentous bacteria; iron mineral
1. Introduction Adhesion of microorganisms to living surfaces in the sea is a well-known phenomenon that has been documented repeatedly (Wahl, 1989; Prieur, 1991; Carman and Dobbs, 1997). Many marine phyla have been reported to possess microorganisms on their external surface, from a few bacterial cells to complex microbial communities featuring bacteria, protozoa and fungi. In the description of such microbe– metazoan interactions, the metazoan is generally called a basibiont, and microbes are called epibionts (Wahl, 1989). Microbial epibionts are generally ignored in the description of marine organisms. However, they may have profound effects on basibiont biology. For * Corresponding author:. E-mail address:
[email protected] (D.C. Gillan).
example the epibiotic diatom Isthmia nervosa provokes a decline in growth and photosynthesis of the red algae Odonthalia floccosa (Ruesink, 1998), the epibiotic bacteria living on the skin of fast-swimming fishes reduce the drag (Sar and Rosenberg, 1987), the epibiotic bacteria on embryos of Homarus americanus produce substances inhibiting the growth of pathogenic fungi (Gil-Turnes and Fenical, 1992), and the sulfur-oxidizing epibiotic bacteria of the nematode Laxus sp. are a food source for the basibiont (Polz et al., 1994). As stressed by Sieburth (1975), “an adequate description of the epibiotic microbiota should become an integral part of the description and study of marine animals”. This study investigates the epibiotic microbiota on the shell of the mudsnail Hydrobia ulvae, a wellknown prosobranch ranging from northern Norway to Senegal and inhabiting the intertidal and shallow subtidal zone (Fretter and Graham, 1994; Hayward
1385-1101/00/$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S1385-110 1(99)00041-6
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Fig. 1. X-ray microanalysis spectra of the biofilm mineral.
and Ryland, 1996). The mudsnail can form dense populations, up to 200 000 ind m 22 (Hauser and Michaelis, 1975). When covered by water the snail crawls over the mud-flat surface, feeding on microalgae and bacteria but preferably on diatoms (Jensen and Siegismund, 1980; Lo´pez-Figueroa and Niell, 1987). It hides below the sediment surface when the tide is low but reappears at the surface as soon as the sediment is covered by water (Vader, 1964; first described by Thamdrup, 1935). A small part of the population may float at the underside of the water surface using a mucous raft for floating and mucous feeding (Newell, 1962; Fretter and Graham, 1994).
2. Materials and methods Of Hydrobia ulvae (Pennant, 1777) 54 live specimens were collected on tidal flats along the coast of
Texel north of ‘De Schorren’ (Wadden Sea, The Netherlands) in June 1997. Another 10 live specimens of H. ulvae were collected in May 1995 on tidal flats near Dangast (Jade Busen, northern Germany). All specimens were collected high in the intertidal zone (near the high-water line). The snails were directly fixed with 70% ethanol (except for the specimens collected in the Jade Busen which were air-dried). For scanning electron microscopy (SEM), the specimens were dehydrated in graded ethanol (90, 100%), dried by the critical-point method using CO2 as transition fluid, mounted, sputter coated with gold, and viewed with an ISI DS 130 SEM microscope operating at 20 kV or a Jeol JSM-6100 SEM microscope operating at 10 kV. For bright-field and Nomarski differential interference contrast (DIC) microscopy, observations were performed on mixed populations of microorganisms that were scraped off the snail shells.
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Fig. 2. Shells of H. ulvae. Scale bar 1 mm.
Fig. 4. C. placentula (AV). SEM, scale bar 10 mm.
To detect the presence of Fe(III) in the epibiotic microbial community we used the Prussian blue method employing 2% ferrocyanide (Na4[Fe(CN)6]) in 1% HCl, and to detect the presence of Fe(II) we used the Turnbull’s blue method employing 2% ferricyanide (Na3[Fe(CN)6]) in 1% HCl (Pearse, 1972). For energy-dispersive X-ray analyses (EDAX), snails were air-dried, mounted and observed under a Jeol superprobe 733 SEM coupled to an EDS (energy dispersive spectrometer) detector. The analysis was done at 25 kV with a sample current of 2.5 nA. EDAX analysis was applied to detect other elements (Fig. 1).
the shell. The coating had a maximum thickness of about 50 mm (Fig. 3), although some specimens presented a thicker coating. In sutures and at the aperture periphery the coating was generally thicker than in the middle regions of the whorls. EDAX analysis indicated that the most abundant elements of the coating were Fe and O. The other elements detected were Mn, Ca, K, S, P, Si, Al and Mg (Fig. 1). Treatment of total shells with acid sodium ferrocyanide led to a strong blue colouration of the shell within seconds; this indicates that Fe(III) was abundant. Treatment with ferricyanide gave no colour reaction, even after 30 min of incubation; this indicates the absence of Fe(II). The coating was very rich in epibiotic diatoms. Two taxa were identified in our material. Both diatom taxa possessed a raphe only on one valve (heterovalvy) and were attached to the substrate with the
3. Results and discussion Thirty-three specimens of H. ulvae from Texel (mean size 5.4 ^ 1.1 mm) (Fig. 2) and 9 specimens from the Jade Busen (mean size 5.3 ^ 1.0 mm) were examined under the SEM. The shells of most snails (95%) were covered with a delicate rust-brown coating that extended from the body whorl to the apex of
Fig. 3. Iron coating on H. ulvae. SEM, scale bar 500 mm.
Fig. 5. C. placentula (RV). SEM, scale bar 10 mm.
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Fig. 6. C. placentula (AV). SEM, scale bar 10 mm.
Fig. 8. A. lemmermannii (RV). SEM, scale bar 1 mm.
raphid valve face. The raphe was a simple slit with straight and parallel sides; a central nodule was present. Type-1 diatoms (Figs. 4–6) were 22.6 ^ 1.7 mm long, and 12.4 ^ 1.1 mm wide. There were 24 ^ 2 transapical striae in 10 mm on both the raphid valve (RV) and araphid valve (AV). The AV was convex with a depressed axial area. The RV was slightly concave. The cingulum of the AV consisted of three girdle bands (Fig. 6). This diatom was identified as Cocconeis placentula. Type-2 diatoms (Figs. 7 and 8) were 12.4 ^ 1.1 mm long, and 4.9 ^ 0.8 mm wide. There were 28 transapical striae in 10 mm on both the RV and AV. The AV and RV appeared flat. This diatom was identified as Achnanthes lemmermannii. Both diatoms covered extensive areas of the shell (Fig. 9). The microbial community also featured aggregates of small coccoid cells. These cells, detected only on
H. ulvae from Texel, were tightly packed and arranged in flat plates adhering to the shell (Figs. 10 and 11). Each cell was about 3 to 7 mm wide. No particular inclusions were detected. These cells presented a thick cell wall that was frequently ironencrusted (Fig. 12). They are possibly cyanobacteria of the genus Pleurocapsa (Entophysalis sensu Drouet) (Humm and Wicks, 1980; Waterbury, 1989). Large trichomes were detected on some H. ulvae from Texel. These trichomes tapered from the base (25–50 mm wide) to the apex (10–15 mm wide) and were 0.2 to 5 mm long (Figs. 13 and 16). Trichomes were multiseriate (two or more rows of cells) (Figs. 14 and 15) and consisted of 10 to 15 mm wide cells. The cells contained 2-mm-wide inclusions (Fig. 15). The cell wall was about 1.25 mm thick. Branching did occur (Fig. 14). These trichomes are possibly cyanobacteria of the order Stigonematales (Castenholz, 1989. Slender filamentous bacteria have also been detected on all specimens (Fig. 17). These filaments were of two types. Type-1 filaments showed
Fig. 7. A. lemmermannii (AV). SEM, scale bar 1 mm.
Fig. 9. Paving of C. placentula. SEM, scale bar 100 mm.
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Fig. 10. Coccoid cells (arrows) and C. placentula. SEM, scale bar 10 mm.
barrel-like cells of constant diameter (1 mm) resembling Leucothrix (Brock, 1989) and Thiothrix (Strohl, 1989); they were about 200 to 400 mm long (Fig. 18). Type-2 filaments showed no distinctive cells and were of constant diameter (0.4–0.6 mm); these filaments were about the same length as type-1 filaments (Fig. 19) and resemble the members of the Cytophagaceae (Reichenbach, 1989). Both types of filaments were frequently encrusted with mineral deposits. The frequency of epibiotic microorganisms was studied under the SEM with 33 H. ulvae from Texel (Table 1). Of the snails examined 85% contained at least one of the above-described microbes in the coating. The most frequent epibionts were C. placentula (72.7%) and slender bacterial filaments (48.5%), followed by A. lemmermannii (27.3%) and large trichomes (15.1%). The frequency of the coccoid cells could not be determined under the SEM because these cells were not easily detected. However, brightfield observations indicated that they were as frequent as C. placentula. The composition of the epibiotic assemblage did not appear related to shell size. When present, C. placentula was very abundant: some specimens of H. ulvae were found completely covered with this species (800 to 1000 diatoms per mm 2 of shell surface) (Figs. 9 and 16). All nine
Fig. 11. Paving of coccoid cells. DIC, scale bar 10 mm.
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Fig. 12. Paving of Fe(III)-encrusted coccoid cells; arrows point to Fe(III) mineral deposits. DIC, scale bar 10 mm.
specimens from the Jade Busen featured C. placentula, A. lemmermannii and slender filaments. Large trichomes were not detected. It is not surprising to find epibiotic microbial communities on shells of H. ulvae because all surfaces in the sea are known to be rapidly colonised by bacteria and diatoms (Cooksey and WigglesworthCooksey, 1995). An early study (Hofker, 1930) already mentioned various protozoans epibiotic on Hydrobia stagnalis in the brackish Zuiderzee (before it became the freshwater IJsselmeer through the closure of the Afsluitdijk in 1932). Hofker (1930) also reports Hydrobia ulvae from the Wadden Sea near Den Helder to be much poorer in epibionts because he found only one ciliate (Cothurnia sp.). What is more surprising is the fact that the epibiotic microbial community is encrusted with a mineral rich in Fe(III), as indicated by the rusty colour of the shells, EDAX analyses, and the positive Prussian blue reaction (Hofker did not mention iron precipitates). Fe(III)-encrusted epibiotic microbial communities have already been described in other marine environments: in the deep-sea, on mussel and limpet shells as well as worm tubes (Jannasch and Wirsen, 1981; Baross and Deming, 1985; Juniper and Tebo,
Fig. 13. Shell of H. ulvae colonised by large trichomes. SEM, scale bar 1 mm.
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Fig. 14. Large trichomes. SEM, scale bar 100 mm.
Fig. 16. Large trichomes and paving of C. placentula. SEM, scale bar 100 mm.
1995), and in the intertidal zone, on the symbiotic bivalve Montacuta ferruginosa (Gillan and De Ridder, 1997; Gillan et al., 1998). The common feature of all these iron-encrusted microbial communities is the presence of numerous filamentous bacteria related to Beggiatoaceae (Beggiatoa and Thiothrix) and Cytophagaceae. Although direct proof of the participation of microorganisms in the formation of ferric minerals in the marine environment is rare (Juniper and Tebo, 1995), it has been shown that the microbial epibionts of M. ferruginosa may participate in iron deposition by their ability to degrade ferric ion organic complexes and their ability to produce extracellular iron-oxidizing factors (Gillan and De Ridder, submitted). It is thus possible that similar processes take place in the biofilm of H. ulvae. The epibiotic microbial community of H. ulvae differs from all the other Fe(III)-encrusted epibiotic communities in that it possesses large numbers of diatoms. Diatoms are frequently observed as epibionts (Holmes, 1985; Howard and Short, 1986; McClatchie et al., 1990; Carman and Dobbs, 1997; Keating and Prezant, 1998; Ruesink, 1998); Cocconeis spp. and Achnanthes spp. are common in the intertidal zone where they grow on various substrates and are ingested by various microphagous grazers such as
limpets (Castenholz, 1963; Nicotri, 1977; Hill and Hawkins, 1991). To our knowledge, it is the first time that diatoms are observed as members of an Fe(III)-encrusted epibiotic microbial community. Interestingly, the adhesive materials of marine fouling diatoms, like those of many marine bacteria, are anionic polysaccharides (Daniel et al., 1987). These substances, also known as exopolymeric substances or EPS, readily bind various metallic species such as iron (McLean et al., 1996). The simultaneous presence of diatoms and Fe(III) minerals on the shell of H. ulvae could be explained by the particular life style of the snail. When the tide is high, snails crawl over the mud-flat surface of the shallow subtidal zone, feeding on diatoms and bacteria (Jensen and Siegismund, 1980; Lo´pez-Figueroa and Niell, 1987). During that time, diatoms and other phototrophic microbes could settle on the shells. Later, at low tide, when the snails burrow into the surface layers of the sediments, the EPS produced by the epibiotic microbes would scavenge the heavy metals present. The mucous substances produced by the snail, like the EPS of microorganisms, may also scavenge heavy metals. The shell epibionts described in this study may influence the environmental conditions of H. ulvae in both a positive and a negative way. Iron precipitation
Fig. 15. Large trichomes. DIC, scale bar 10 mm.
Fig. 17. Slender filaments. SEM, scale bar 10 mm.
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Table 1 Abundance of epibiotic microorganisms on the shell of Hydrobia ulvae from Texel Snail
Fig. 18. Slender filaments of type 1. SEM, scale bar 1 mm.
by some microorganisms in the epibiotic biofilm may remove the toxic Fe(II) ions and sulfide that occur in sediments, as suggested for M. ferruginosa and other invertebrates (Vismann, 1991; Gillan and De Ridder, 1997). In molluscs such as Mytilus edulis, bacterial microborers are known to decompose the periostracum and the organic shell matrix, leading to shell dissolution (Knauth-Ko¨hler et al., 1996). Although some microbes described in this work are possibly shell microborers, the progressive iron encrustation of the shell could protect it against microborer activity. The epibiotic bacteria could also produce toxic compounds or act as chemical camouflage, and thus protect snails against predators or parasites which identify prey by chemical cues (Wahl, 1989); this of course will not help against the main predators of Hydrobia in the Wadden Sea: birds such as knot, shelduck, pintail and dunlin (Wolff, 1983). It is also possible that epibionts influence the fixation of egg capsules on the shell (Fish and Fish, 1974) or the buoyancy of the snails; for example, heavily ironencrusted shells are probably heavier to carry. In this study we show that many iron-encrusted epibionts are present on H. ulvae. The epibionts must be taken into account when the host ecology is studied. Future research could for example concentrate more explicitly on the influence
Size (mm)
Cocc.
Achn
Sl. fil.
Large fil.
1 3.00 111 1 1 X 2 4.25 1 1 X X 3 4.25 X X X X 4 4.25 111 X 1 X 5 4.75 1 1 X X 6 4.75 1 X 1 X 7 5.00 1 1 1 X 8 5.00 1 X X X 9 5.00 1 X X X 10 5.25 X X X X 11 5.25 1 1 1 X 12 5.5 1 1 1 1 13 5.5 111 1 X 1 14 5.5 X X X X 15 5.5 1 X 1 1 16 5.5 X X 1 X 17 5.75 11 11 1 X 18 5.75 1 X X X 19 5.75 X X 1 X 20 6.00 1 X X X 21 6.00 1 X 1 1 22 6.00 111 X 1 X 23 6.25 X X X X 24 6.25 X X X X 25 6.25 111 X X X 26 6.5 X X 1 X 27 6.5 1 X X X 28 6.75 X X 1 X 29 6.75 1 X X X 30 7.00 X X X X 31 7.00 1 X 1 X 32 7.00 1 X 1 X 33 7.5 1 X X X Mean values: 5:67 ^ 0:98 72.7% 27.3% 48.5% 15.1% Cocc. Cocconeis; Achn. Achnanthes; Large fil. large filaments; Sl.fil. slender filaments. 111 . 50% of shell surface covered; 11 , 50% of shell surface covered; 1 , 1% of shell surface covered; X not detected.
of epibionts on the fitness of the snails, or on the composition of the epibiotic coating according to the habitat of the snails (near the low- or the highwater line).
Acknowledgements Fig. 19. Slender filaments of type 2 (arrow). SEM, scale bar 1 mm.
We thank Dr H. de Wolf for his help in the identification of diatoms. The research was supported by a
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FRIA grant to D.C.G. (ref. 940733) and a FRFC grant to C.D.R. (ref. 2-4510-96). This is a contribution of the ‘Centre Interuniversitaire de Biologie Marine’ (CIBIM).
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