Contrasting controls on seasonal and spatial distribution of marine cable bacteria (Candidatus Electrothrix) and Beggiatoaceae in seasonally hypoxic Chesapeake Bay

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 to Candidatus Electrothrix communis, 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 multiple Candidatus Electrothrix phylotypes, 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

CABLE BACTERIA AND THEIR MICROBIAL ASSOCIATIONS IN LAB-INCUBATED SEDIMENT FROM CHESAPEAKE BAY

Cable bacteria (Ca. Electrothrix) are long, filamentous, multicellular bacteria that grow in marine sediments and couple sulfur oxidation to oxygen reduction over centimeter-scale distances via an enigmatic long-distance electron transport mechanism. They can grow to tremendous densities and strongly modify the sediment environment in multiple ways, including efficient sulfide removal, stimulation of sulfate reduction, and alteration of porewater pH distribution. In this thesis, I asked if cable bacteria can influence the sympatric microbial community composition and activity, using a time-series manipulation experiment. As anticipated, based on their influence on sediment geochemistry, cable bacteria growth was associated with the stimulation of several genera of sulfate-reducing bacteria, and a sulfur-disproportionating genus (Desulfocapsa). I observed a positive relationship with the OM27 clade of the predatory Bdellovibrionota. Finally, I detected evidence of interaction with two chemoautotrophic sulfur oxidizers (Thiogranum, Sedimenticola), which are good candidates for further examination of potential electrical connection with cable bacteria