Cycloclasticus spp. bacteria are not fussy eaters: even short-chain hydrocarbons will do!

Cycloclasticus is a genus of obligate oil-degrading bacteria (class Gammaproteobacteria), capable of metabolising hydrocarbons via aerobic oxidative pathways (please refer to “Microbial sediments” lecture). Cultured Cycloclasticus spp. have the ability to degrade Polycyclic Aromatic Hydrocarbons (PAHs), a group of organic pollutants which partly make up the hydrocarbon mixture in petroleum. Cycloclasticus spp. OTUs have been identified in metagenomes from Deepwater Horizon (DWH) oil spill samples and were enriched in SIP experiments using ¹³C-labelled PAH substrates (Dombrowski et al., 2016). For these reasons, their role in hydrocarbon biodegradation is well acknowledged.
Rubin-Blum et al. used a meta –omics approach to identify hydrocarbon metabolism pathways in metagenomes, metatranscriptomes and metaproteomes of symbiotic Cycloclasticus spp. associated with two deep sea bivalve congeners (gills of Bathymodiolus heckerae and B. brooksi) and two sponge species. Each host species (except for B. brooksi) harboured distinct host-specific Cycloclasticus spp. phylotypes, whose abundance ranged between 4.1 and 10.7 % of the total bacterial 16S rDNA barcodes. Cycloclasticus spp. symbionts were intracellularly located in B. heckerae gill bacteriocytes, as revealed by FISH. Notably, genes involved in PAH metabolism were not identified in Cycloclasticus spp. genomes and transcriptomes, and a SIP experiment confirmed the inability of Cycloclasticus spp. B. heckerae symbionts to metabolise PAHs (¹⁴C-labelled naphthalene). On the other hand, a highly expressed set of genes (both at the transcriptional and protein levels) putatively involved in the oxidative short-chain alkane (C2-C4) metabolism were identified in all three host species.
The results provide convincing –omics evidence for an expanded Cycloclasticus hydrocarbon substrate repertoire, thus not just limited to PAHs, as suggested by a previous report (Valentine et al., 2010). Importantly, the authors measured short-chain alkanes present in gas bubbles and asphalt gas hydrates at the sites of sampling, showing that they are present in significant amounts. Moreover, both mussel and sponge hosts are filter-feeders, so it is not unreasonable to hypothesise that their water-filtering activity would expose their hydrocarbon-degrading symbionts to increased levels of short-chain alkanes, therefore fuelling Cycloclasticus spp. metabolism, as the authors pointed out. As well as in natural hydrocarbon seeps, short-chain alkanes are present in anthropogenic oil spill-derived plumes, especially in the initial stages, and are believed to be among the first substrates utilised by hydrocarbon-degrading bacteria (Valentine et al., 2010).
The study provides an excellent insight into the metabolism of oil-degrading bacteria which are supported by a natural source of hydrocarbons. Future investigations should explore the significance of Cycloclasticus spp. bacteria to their animal hosts, and aim to identify and quantify the implications of their metabolism for the carbon cycle. On a related note, a previous study suggested that metabolic complementation could be a likely explanation for the occurrence of “pathway gaps” in metagenomic datasets from DWH spill plume-associated bacteria (Dombrowski et al., 2016). Thus, it would be interesting to investigate the eventuality and extent of metabolic complementation among Cycloclasticus spp. and other bacterial symbionts.

Reviewed article:
Rubin-Blum, M., Antony, C. P., Borowski, C., Sayavedra, L., Pape, T., Sahling, H., Bohrmann, G., Kleiner, M., Redmond, M. C., Valentine, D. L. & Dubilier, N. (2017) 'Short-chain alkanes fuel mussel and sponge Cycloclasticus symbionts from deep-sea gas and oil seeps'. Nature Microbiology, 2, pp. 17093.

References
Dombrowski, N., Donaho, J. A., Gutierrez, T., Seitz, K. W., Teske, A. P. & Baker, B. J. (2016) 'Reconstructing metabolic pathways of hydrocarbon-degrading bacteria from the Deepwater Horizon oil spill'. Nature Microbiology, 1, pp. 16057.

Valentine, D. L., Kessler, J. D., Redmond, M. C., Mendes, S. D., Heintz, M. B., Farwell, C., Hu, L., Kinnaman, F. S., Yvon-Lewis, S., Du, M., Chan, E. W., Tigreros, F. G. & Villanueva, C. J. (2010) 'Propane Respiration Jump-Starts Microbial Response to a Deep Oil Spill'. Science, 330 (6001), pp. 208.