Microbial succession in a marine sediment: Inferring interspecific microbial interactions with marine cable bacteria

Abstract

Cable bacteria are long, filamentous, multicellular bacteria that grow in marine sediments and couple sulfide oxidation to oxygen reduction over centimetre-scale distances via long-distance electron transport. Cable bacteria can strongly modify biogeochemical cycling and may affect microbial community networks. Here we examine interspecific interactions with marine cable bacteria (Ca. Electrothrix) by monitoring the succession of 16S rRNA amplicons (DNA and RNA) and cell abundance across depth and time, contrasting sediments with and without cable bacteria growth. In the oxic zone, cable bacteria activity was positively associated with abundant predatory bacteria (Bdellovibrionota, Myxococcota, Bradymonadales), indicating putative predation on cathodic cells. At suboxic depths, cable bacteria activity was positively associated with sulfate-reducing and magnetotactic bacteria, consistent with cable bacteria functioning as ecosystem engineers that modify their local biogeochemical environment, benefitting certain microbes. Cable bacteria activity was negatively associated with chemoautotrophic sulfur-oxidizing Gammaproteobacteria (Thiogranum, Sedimenticola) at oxic depths, suggesting competition, and positively correlated with these taxa at suboxic depths, suggesting syntrophy and/or facilitation. These observations are consistent with chemoautotrophic sulfur oxidizers benefitting from an oxidizing potential imparted by cable bacteria at suboxic depths, possibly by using cable bacteria as acceptors for electrons or electron equivalents, but by an as yet enigmatic mechanism.

FIGURE 1

Cable bacteria abundance through depth during the incubation experiment with Chesapeake Bay sediment at 6 time points (Days 3, 6, 10, 14, 20, and 46) as indicated at the figure top. Percentage of amplicons affiliated to Ca. Electrothrix according to (A) RNA‐based and (B) DNA‐based 16S rRNA gene amplicon sequencing. (C) Direct counts of cable bacteria using FISH oligoprobe DSB‐706 (‘DSB cell abundance’). (D) The ratio of RNA‐based to DNA‐based amplicon reads affiliated to Ca. Electrothrix.

FIGURE 2

Microsensor profiles of O₂ (red), pH (black), and H₂S (blue) across time. Data from sediment cores without barrier filters are depicted in panels (A)–(F), and show the geochemical fingerprint of increasing cable bacteria activity between Days 10 and 20. Data from cores with barrier filters, embedded to inhibit downward growth of cable bacteria, are depicted in panels (G)–(J). Shaded regions indicate sections of sediment core sampled for geochemistry, cell counts, and amplicon sequencing.

FIGURE 3

Principal coordinates analysis (PCoA) on the Bray–Curtis dissimilarity distance of RNA‐based 16S rRNA gene amplicon analysis. The symbol shape indicates sample types (samples from sediment cores with embedded barrier filters; samples without barrier filters and >5% Ca. Electrothrix read abundance; samples without barrier filters and <5% Ca. Electrothrix). Colours indicate sampling depth. Ellipses are drawn around three main clusters (surface samples, subsurface samples with <5% cable bacteria read abundance, subsurface samples with >5% cable bacteria read abundance).

FIGURE 4

Among samples from the sediment surface (0–0.5 cm depth), the temporal changes in the fractional read abundance of RNA‐based amplicon sequencing times cell counts (‘FRAxC activity’) of the microbial taxa that were robustly negatively (red) or positively (blue) correlated with Ca. Electrothrix. Taxonomic identities are included for each ASV at the lowest known phylogenetic resolution. The size of the bubble indicates the magnitude of the FRAxC activity.

FIGURE 5

Among subsurface suboxic and anoxic samples (0.5–2.0 cm depth), the temporal changes in FRAxC activity of the microbial taxa that were robustly negatively (red) or positively (blue) correlated with Ca. Electrothrix. Taxonomic identities are included for each ASV at a known phylogenetic resolution.

FIGURE 6

Conceptual diagrams of potential microbial interactions with marine cable bacteria. These include (A) predator–prey interactions, for example by obligate intracellular predators affiliated to Bdellovibrionota and/or swarming facultative predators affiliated to Myxococcota and Bradymonadales; (B) cable bacteria acting as ecosystem engineers by altering local geochemistry, such as stimulating bacteria with high iron requirements (e.g., Magnetovibrio) by acidic dissolution of FeS, or altering distribution of acidity, promoting alkaliphilic bacteria at the sediment surface (e.g., Thioalkalispira) and impeding sulfur disproportionators (e.g., Desulfocapsa) by acidification of the suboxic zone; (C) competitive interactions such as with single celled sulfur oxidizers (e.g., Thiogranum, Sedimenticola), and (D) syntrophic or facilitative interactions, for example as hypothesized for putative chemoautotrophic sulfur oxidizers potentially benefitting energetically from the activity of cable bacteria (e.g., Thiogranum, Sedimenticola). Cable bacteria are illustrated as green multicellular filaments. The overlying oxygenated water is illustrated as blue, and the sediment, with increasingly reducing conditions at depth, is illustrated by brown to black gradient. Panel (B) includes a typical depth profile of pH and sulfide removal attributable to cable bacteria long distance electron transport activity.