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Nanohaloarchaea as beneficiaries of xylan degradation by haloarchaea
La Cono, Violetta; Messina, Enzo; Reva, Oleg N.; Smedile, Francesco; La Spada, Gina; Crisafi, Francesca; Marturano, Laura; Miguez, Noa; Ferrer, Manuel; Selivanova, Elena A.; Golyshina, Olga V.; Golyshin, Peter N.; Rohde, Manfred; Krupovic, Mart; Merkel, Alexander Y.; Sorokin, Dimitry Y.; Hallsworth, John E.; Yakimov, Michail M.
Climate change, desertification, salinisation of soils and the changing hydrology
of the Earth are creating or modifying microbial habitats at all scales
including the oceans, saline groundwaters and brine lakes. In environments
that are saline or hypersaline, the biodegradation of recalcitrant plant and animal
polysaccharides can be inhibited by salt-induced
microbial stress and/or
by limitation of the metabolic capabilities of halophilic microbes. We recently
demonstrated that the chitinolytic haloarchaeon Halomicrobium can serve as
the host for an ectosymbiont, nanohaloarchaeon ‘Candidatus Nanohalobium
constans’. Here, we consider whether nanohaloarchaea can benefit from the
haloarchaea-mediated
degradation of xylan, a major hemicellulose component
of wood. Using samples of natural evaporitic brines and anthropogenic
solar salterns, we describe genome-inferred
trophic relations in two extremely
halophilic xylan-degrading
three-member
consortia. We succeeded in genome
assembly and closure for all members of both xylan-degrading
cultures
and elucidated the respective food chains within these consortia. We provide
evidence that ectosymbiontic nanohaloarchaea is an active ecophysiological
component of extremely halophilic xylan-degrading
communities (although
by proxy) in hypersaline environments. In each consortium, nanohaloarchaea
occur as ectosymbionts of Haloferax, which in turn act as scavenger of oligosaccharides produced by xylan-hydrolysing
Halorhabdus. We further
obtained and characterised the nanohaloarchaea–host
associations using
microscopy, multi-omics
and cultivation approaches. The current study also
doubled culturable nanohaloarchaeal symbionts and demonstrated that these
enigmatic nano-sized
archaea can be readily isolated in binary co-cultures
using an appropriate enrichment strategy. We discuss the implications of
xylan degradation by halophiles in biotechnology and for the United Nation's
Sustainable Development Goals.
Description:
DATA AVAILABILITY STATEMENT :
All statements regarding data availability, finding resources
and conflict of interest disclosure have been
provided.
DATA DEPOSITION :
All (meta)genomic and transcriptomic information is
available under GenBank BioProject ID PRJNA865582;
BioSamples SAMN30630960, SAMN30630938,
SAMN30630946, SAMN30631035, SAMN30630966,
SAMN30631033, SAMN30120999, SAMN30121000,
SAMN30121001, SAMN30121002, SAMN30121003
and SAMN30121004; genome accession no. CP104322
for Halorhabdus sp. SVX81, genome accession no.
CP104395 for Ca. Nanohalococcus occultus SVXNc,
genome accession nos. CP104741 (chromosome),
CP104742 (plasmid 1), CP104743 (plasmid 2) and
CP104744 (plasmid 3) for Haloferax lucertense SVX82;
genome accession no. CP107254 for Halorhabdus
sp. BNX81, genome accession no. CP107255 for Ca.
Nanohalovita haloferacivicina BNXNv, genome accession
nos. CP106966 (chromosome), CP106967 (plasmid
1), CP106968 (plasmid 2), CP106969 (plasmid 3)
and CP106970 (plasmid 4) for Haloferax lucertense
BNX82. Transcriptomic raw data are available under
accession SRR21676140-SRR216761401.
The mass spectrometry proteomics data have been deposited in
the ProteomeXchange Consortium via the PRIDE partner
repository with the data set identifier PXD036877.