Differential lysis of sedimentary bacteria by Arenicola marina L.: examination of cell wall structure and exopolymeric capsules as correlates
Introduction
Bacteria in marine sediments play key roles in biogeochemical cycling and food web dynamics. Research effort has increased considerably during the last two decades, in so far as we now have a fair degree of predictive ability regarding the more quantitative aspects of the ecology of these bacteria, such as densities, biomass, and production rates (e.g., Cole et al., 1988, Deming and Baross, 1993). Significantly less is known about community composition and those factors which structure benthic microbial communities.
Questions regarding microbial loops have been more intensively studied in planktonic situations. There are parallels, however, in that study of bacterioplankton community structure has also lagged behind that of the more quantitative questions. Recent work, however, has begun to focus more on community structure and driving mechanisms (Jurgens and Gude, 1994). For instance, grazing by nanoflagellates has been identified as the main bacterial loss factor (Fenchel, 1982, Pace, 1988, Jurgens and Gude, 1994) which can at times balance production (Sherr and Sherr, 1984, Wright and Coffin, 1984, del Giorgio et al., 1996). However, protistan grazing also appears to play a role in the structuring of size and species composition of planktonic bacteria (e.g. Gude, 1989, Jurgens and Gude, 1994). Drastic changes in both taxonomic composition (Gude, 1979, Bianchi, 1989, Simek et al., 1997) and size structure (Shikano et al., 1990, Sommaruga and Psenner, 1995) have been observed due to differential predation by flagellates. Furthermore, mechanisms of differential removal, such as selective ingestion (see Jurgens and Gude, 1994for review, Sherr et al., 1992; Pernthaler et al., 1997) and differential digestion (see Jurgens and Gude, 1994for review, Gonzalez et al., 1990), have been identified.
Although it is tempting to assume that the cited advances in the study of planktonic microbial loops can be applied to benthic systems, certain fundamental differences may preclude such a practice. One important difference is that most sedimentary bacteria are attached to sediment grains or other relatively large particles (Dye, 1983, Ellery and Schleyer, 1984) whereas the water column is dominated by free-living forms (Gude, 1988, Jurgens and Gude, 1994, Bidle and Fletcher, 1995). Attachment inhibits consumption by small grazers such as flagellates (Caron, 1987), yet makes bacteria more available to macrofaunal grazers (Schoenberg and Maccubin, 1985, Lawrence et al., 1993). Thus, the importance of macrofaunal grazers should be relatively more important to bacterial communities in benthic as compared to planktonic habitats. Extensive biofilms that normally envelop attached bacteria may also result in greater resistance to digestion by either protists or macrofauna, but the protection against protists should be relatively greater since both ingestion and digestion would be hindered. These differences may explain why protozoan grazers have generally been found to be incapable of balancing bacterial production in sediments (Kemp, 1988, Alongi, 1989, Epstein and Shiaris, 1992, Starink et al., 1996), in contrast to the situation in the water column.
Neither is it clear, however, that deposit-feeding macrofauna can significantly counter bacterial production in sediments. In the majority of studies that have examined whether the impact of deposit feeding is significant, a gross imbalance between bacterial production and deposit-feeder consumption has been found (e.g. Kemp, 1987, Kemp, 1990, Plante et al., 1989). This inability of deposit feeders to control microbes is almost certainly due to insufficient feeding rate, rather than to shortcomings in digestive efficiencies, which usually exceed 50% (Cammen, 1980, Duchene et al., 1988, Plante et al., 1989, Grossmann and Reichardt, 1991) and can approach 100% (e.g. Duchene et al., 1988). Under special circumstances (e.g. when feeding is spatially restricted), however, ingestion and digestive efficiency can reach sufficient magnitudes as to influence bacterial abundances and growth rates in sediments (e.g. Moriarty et al., 1985, Grossmann and Reichardt, 1991).
Moreover, compositional differences between the bacterial communities of ingested sediments and those of egesta have been demonstrated (e.g., Findlay and White, 1983, Duchene et al., 1988, Dobbs and Guckert, 1988). Lysis of diverse sedimentary strains of bacteria by deposit-feeing macrofauna may occur at different rates, thus altering the composition of bacteria in feces and surrounding sediments. Differential digestion cannot clearly be concluded from the results of these previous studies, however, since growth in the hindgut of the deposit feeders can be significant (Deming and Colwell, 1982, Plante et al., 1989) and may vary among bacterial strains.
A related question pertains to the inefficiency of bacteriolysis by deposit feeders. On average, only ≃60% of ingested bacteria are digested during gut transit (see Kemp, 1990, and references therein). It is unclear whether inefficiencies are due to differences in lytic susceptibilties among bacterial strains or whether individuals within strains vary in susceptibility because of differences in growth stage, strength of attachment to particulates or the quantity or quality of exopolymer secretions.
The primary purpose of this study was to determine whether various sedimentary bacterial isolates were equally susceptible to digestion by the digestive fluids of deposit feeders. The secondary goal was to begin to ascertain the potential mechanisms of differential digestion. Specifically, the potentially important factors of cell wall type and exopolymer capsule production were examined.
Section snippets
Specimen collection
Samples of digestive fluid from the marine deposit-feeding polychaete, Arenicola marina L., were collected from Pratt's Island, Maine and pooled. Fluids were taken only from the midgut of the lugworm; dissection procedures and designations of various gut sections for A. marina have been provided previously (Plante and Mayer, 1994).
Bacterial strains were isolated from sediments and lugworm feces. Initial isolations were on either Marine Broth 2216 agar medium (Difco; Detroit, MI, USA), or this
Results
Lytic susceptibility of environmental isolates varied significantly among strains (Fig. 1; P<0.0001, ANOVA). Eleven of the 43 strains exhibited lytic susceptibility significantly greater than zero (P<0.05, Normal test).
During the course of this study two strains were lost in culture so characterization of biochemical or structural features are incomplete (see SS-8 and SS-113 in Table 1 and Table 2). In addition, one strain, SS-109, was initially identified as gram-negative and was susceptible
Discussion
The majority of bacterial isolates tested were resistant to lysis by the gut fluids of A. marina. These findings run counter to expectations based on the prior studies of Chua and Brinkhurst (1973), Prieur (1981), and Seiderer et al. (1984), who found that the majority of bacterial types were digested by various benthic invertebrates (oligochaetes, clams, and mussels, respectively). A partial explanation, no doubt, relates to the nature of our assay. Within the gut, the ratio of digestive
Acknowledgements
We wish to thank S. Hymel and two anonymous reviewers for constructive reviews of earlier drafts. Financial support was provided by NSF grant OCE 95-04505 and a College of Charleston Research and Development Grant.
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