Arcobacteraceae
are ubiquitous mixotrophic bacteria playing important roles in carbon, nitrogen, and sulfur cycling in global oceans
Authors: Li Jianyang , Xiang Shizheng , Li Yufei , Cheng Ruolin , Lai Qiliang , Wang Liping , Li Guizhen , Dong Chunming , Shao Zongze 
Published: June 2024

ABSTRACT

Mixotrophy is an important trophic strategy for bacterial survival in the ocean. However, the global relevance and identity of the major mixotrophic taxa remain largely elusive. Here, we combined phylogenetic, metagenomic, and metatranscriptomic analyses to characterize ubiquitous
Arcobacteraceae
based on our deep-sea
in situ
incubations and the global data. The phylogenomic tree of
Arcobacteraceae
is divided into three large clades, among which members of clades A and B are almost all from terrestrial environments, while those of clade C are widely distributed in various marine habitats in addition to some terrestrial origins. All clades harbor genes putatively involved in chitin degradation, sulfide oxidation, hydrogen oxidation, thiosulfate oxidation, denitrification, dissimilatory nitrate reduction to ammonium, microaerophilic respiration, and metal (iron/manganese) reduction. Additionally, in clade C, more unique pathways were retrieved, including thiosulfate disproportionation, ethanol fermentation, methane oxidation, fatty acid oxidation, cobalamin synthesis, and dissimilatory reductions of sulfate, perchlorate, and arsenate. Within this clade, two mixotrophic Candidatus genera represented by UBA6211 and CAIJNA01 harbor genes putatively involved in the reverse tricarboxylic acid pathway for carbon fixation. Moreover, the metatranscriptomic data in deep-sea
in situ
incubations indicated that the latter genus is a mixotroph that conducts carbon fixation by coupling sulfur oxidation and denitrification and metabolizing organic matter. Furthermore, global metatranscriptomic data confirmed the ubiquitous distribution and global relevance of
Arcobacteraceae
in the expression of those corresponding genes across all oceanic regions and depths. Overall, these results highlight the contribution of previously unrecognized
Arcobacteraceae
to carbon, nitrogen, and sulfur cycling in global oceans.

IMPORTANCE

Marine microorganisms exert a profound influence on global carbon cycling and ecological relationships. Mixotrophy, characterized by the simultaneous utilization of both autotrophic and heterotrophic nutrition, has a significant impact on the global carbon cycling. This report characterizes a group of uncultivated bacteria
Arcobacteraceae
that thrived on the “hot time” of bulky particulate organic matter and exhibited mixotrophic strategy during the
in situ
organic mineralization. Compared with clades A and B, more unique metabolic pathways were retrieved in clade C, including the reverse tricarboxylic acid pathway for carbon fixation, thiosulfate disproportionation, methane oxidation, and fatty acid oxidation. Global metatranscriptomic data from the Tara Oceans expeditions confirmed the ubiquitous distribution and extensive transcriptional activity of
Arcobacteraceae
with the expression of genes putatively involved in carbon fixation, methane oxidation, multiple sulfur compound oxidation, and denitrification across all oceanic regions and depths.