Abstract

ABSTRACTA paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many aspects of a host’s phenotype and evolution. In the process, an era of “holobiont” research has emerged to investigate the intricate network of interactions between a host and its symbiotic microbial consortia. Marine sponges are early-diverging metazoa known for hosting dense, specific, and often highly diverse microbial communities. Here we synthesize current thoughts about the environmental and evolutionary forces that influence the diversity, specificity, and distribution of microbial symbionts within the sponge holobiont, explore the physiological pathways that contribute to holobiont function, and describe the molecular mechanisms that underpin the establishment and maintenance of these symbiotic partnerships. The collective genomes of the sponge holobiont form the sponge hologenome, and we highlight how the forces that define a sponge’s phenotype in fact act on the genomic interplay between the different components of the holobiont.

Highlights

  • DEFINING THE SPONGE HOLOGENOMESponges (phylum Porifera) are among the most ancient of the extant multicellular organisms, evolving over 580 million years ago and encompassing over 8,600 formally described and 15,000 estimated species that are distributed across shallow and deepwater habitats from the tropics to the poles [1]

  • A paradigm shift has recently transformed the field of biological science; molecular advances have revealed how fundamentally important microorganisms are to many aspects of a host’s phenotype and evolution

  • ® mbio.asm.org mined the abundances of bacteria, archaea, chloroflexi, actinobacteria, cyanobacteria, and poribacteria and discerned notable differences that relate to the overall microbial abundance within the host [18,19,20,21,22]

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Summary

DEFINING THE SPONGE HOLOGENOME

Sponges (phylum Porifera) are among the most ancient of the extant multicellular organisms, evolving over 580 million years ago and encompassing over 8,600 formally described and 15,000 estimated species that are distributed across shallow and deepwater habitats from the tropics to the poles [1]. ® mbio.asm.org mined the abundances of bacteria, archaea, chloroflexi, actinobacteria, cyanobacteria, and poribacteria and discerned notable differences that relate to the overall microbial abundance within the host [18,19,20,21,22] While this HMA-LMA dichotomy is a topic of current research, little is yet known about why particular sponge species host so few symbionts and whether the interactions within the hologenomes of LMA species are fundamentally different from those of their HMA counterparts. The application of host-symbiont network analysis to 16S rRNA gene surveys can provide a valuable approach for exploring ecological and evolutionary dynamics within holobionts These tools have only recently been applied to sponge holobionts and are generating interesting insights into the complex web of interactions and species distributions that can occur in sponges [38, 39] as well as in other symbiotic systems [40]. Unique insights into sponge-symbiont interactions and distributions are expected to be revealed by the utilization of such networking tools

PROCESSES OF SYMBIONT TRANSMISSION AND ACQUISITION
PHYSIOLOGICAL INTERACTIONS WITHIN THE SPONGE HOLOGENOME
Feeding studies have certainly confirmed that sponges are able
ENVIRONMENTAL ADAPTATION OF THE SPONGE HOLOGENOME
FUNCTIONAL CONVERGENCE AND EVOLUTION OF THE SPONGE HOLOGENOME
Findings
CONCLUSIONS
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