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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. 

Abstract Marine cable bacteria (Candidatus Electrothrix) and large colorless sulfur‐oxidizing bacteria (e.g., Beggiatoaceae) are widespread thiotrophs in coastal environments but may exert different influences on biogeochemical cycling. Yet, the factors governing their niche partitioning remain poorly understood. To map their distribution and evaluate their growth constraints in a natural setting, we examined surface sediments across seasons at two sites with contrasting levels of seasonal oxygen depletion in Chesapeake Bay using microscopy coupled with 16S rRNA gene amplicon sequencing and biogeochemical characterization. We found that cable bacteria, dominated by a single phylotype closely affiliated toCandidatus Electrothrixcommunis, flourished during winter and spring at a central channel site which experiences summer anoxia. Here, cable bacteria density was positively correlated with surface sediment chlorophyll, a proxy of phytodetritus sedimentation. Cable bacteria were also present with a lower areal density at an adjacent shoal site which supports bioturbating macrofauna. Beggiatoaceae were more abundant at this site, where their biomass was positively correlated with sediment respiration, but additionally potentially inhibited by sulfide accumulation which was evident during one summer. A springtime phytodetritus sedimentation event was associated with a proliferation of Beggiatoaceae and multipleCandidatus Electrothrixphylotypes, with cable bacteria reaching 1000 m length cm⁻². These observations indicate the potential impact of a spring bloom in driving a hot moment of cryptic sulfur cycling. Our results suggest complex interactions between benthic thiotroph populations, with bioturbation and seasonal oscillations in bottom water dissolved oxygen, sediment sulfide, and organic matter influx as important drivers of their distribution.