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

Abstract

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
Volume16
Issue number4
DOIs
StatePublished - Apr 2022

Bibliographical note

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

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Microbiology

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