Division of labor and growth during electrical cooperation in multicellular cable bacteria

Abstract

Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with 13C (bicarbonate and propionate) and 15N-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the “community service” performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms.

Quantification of Cable Bacteria in Marine Sediments via qPCR

“…The cell specific oxygen consumption rate of cable bacteria in the oxic zone calculated from the cathodic oxygen consumption, the oxygen penetration depth (∼1 mm; Figure 1E ) and qPCR enumerated cable bacteria is 69 ± 58 fmol O 2 cell –1 day –1 , which is within the same order of magnitude as the value of 36 fmol O 2 cell –1 day –1 reported by Schauer et al (2014) . Measurements of the oxygen reduction capacity of cable bacteria using cyclic voltammetry resulted in a rate of 6.1 pmol O 2 cell –1 day –1 (at 50 μM O 2 ; Geerlings et al, 2020 ), hence the potential capacity for oxygen reduction is approximately a hundred times larger than the actual rates in sediment incubations.…”

“…The pathway by which oxygen is reduced in cable bacteria is currently unknown. Recent 13 C and 15 N labeling studies have shown that cells in the oxic zone of the sediment show very little or no carbon or nitrogen assimilation, implying that oxygen reduction in cable bacteria is not coupled to energy conservation (Geerlings et al, 2020). Moreover, no terminal oxidases could be identified in cable bacteria genomes and it was hypothesized that cable bacteria reduce oxygen via periplasmic cytochromes (Kjeldsen et al, 2019).…”

Oxygen consumption of individual cable bacteria

“…Cable bacteria were observed to generate distinct distortions of the oxic-anoxic interface in gradient systems, and we realized that this allowed measurements of the rate and location of oxygen consumption in individual bacteria. This novel approach was used in the present study to directly test the hypothesis that cable bacteria can limit oxygen reduction to a few cells with high consumption rates (10,12). Data from independent individuals of a single-strain population established in seminatural gradient systems were collected until robust measures of the variability and biomass-specific capacity of oxygen consumption were obtained.…”

Mutational meltdown of microbial altruists in Streptomyces coelicolor colonies

“…Division of labor allows populations of individuals to more efficiently carry out functions that are mutually incompatible 25,26 . In microbes, division of labor can facilitate biofilm formation 25,27,28 , energy transfer 29 , and coordinated metabolism 13,30 , among other behaviors. In some cases, division of labor leads to sub-populations of cells that carry out functions that are lethal to themselves but that benefit the entire colony 31 .…”