Lineage-specific energy and carbon metabolism of sponge symbionts and contributions to the host carbon pool

I. Burgsdorf, S. Sizikov, V. Squatrito, M. Britstein, B. M. Slaby, C. Cerrano, K. M. Handley, L. Steindler

Research output: Contribution to journalArticlepeer-review


Marine sponges host a wide diversity of microorganisms, which have versatile modes of carbon and energy metabolism. In this study we describe the major lithoheterotrophic and autotrophic processes in 21 microbial sponge-associated phyla using novel and existing genomic and transcriptomic datasets. We show that the main microbial carbon fixation pathways in sponges are the Calvin–Benson–Bassham cycle (energized by light in Cyanobacteria, by sulfur compounds in two orders of Gammaproteobacteria, and by a wide range of compounds in filamentous Tectomicrobia), the reductive tricarboxylic acid cycle (used by Nitrospirota), and the 3-hydroxypropionate/4-hydroxybutyrate cycle (active in Thaumarchaeota). Further, we observed that some sponge symbionts, in particular Acidobacteria, are capable of assimilating carbon through anaplerotic processes. The lithoheterotrophic lifestyle was widespread and CO oxidation is the main energy source for sponge lithoheterotrophs. We also suggest that the molybdenum-binding subunit of dehydrogenase (encoded by coxL) likely evolved to benefit also organoheterotrophs that utilize various organic substrates. Genomic potential does not necessarily inform on actual contribution of autotrophs to light and dark carbon budgets. Radioisotope assays highlight variability in the relative contributions of photo- and chemoautotrophs to the total carbon pool across different sponge species, emphasizing the importance of validating genomic potential with physiology experimentation.

Original languageEnglish
Pages (from-to)1163-1175
Number of pages13
JournalISME Journal
Issue number4
StatePublished - Apr 2022

Bibliographical note

Funding Information:
The authors thank the Inter-University Institute (IUI) in Eilat, Israel, for their technical support in SCUBA dives and laboratory availability for physiology experiments. LS wishes to warmly thank Prof. Sven Beer and Prof. Micha Ilan for support with the experiments on T. swinhoei. Dr. Eyal Rahav and Dr. Natasha Belkin are thanked for advice on radioactive measurements and calculations. Dr. Stefan Green, director of the DNA Services Facility at the University of Illinois at Chicago (UIC) is thanked for useful comments and suggestions on sequencing strategies. The authors also thank Igor Chebotar, high performance computing system (HPC) administrator of the faculty of natural sciences at University of Haifa for his technical support in software and hardware assistance.

Funding Information:
This work was supported by funds provided by the Israel Science Foundation [Grant No. 1243/16] and by the Gordon and Betty Moore Foundation, through Grant GBMF9352.

Publisher Copyright:
© 2021, The Author(s).

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics


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