The Rhythm of Many: Biological Rhythms in the Marine Environment, From Macro-Scale Planktonic Ecosystems to Micro-Scale Holobionts

Olivia H Hewitt,Hisham M Shaikh

doi:10.3389/fmars.2021.744169

Abstract

Daily environmental oscillations that follow Earth’s rotation around the Sun set a metronome for life, under which all organisms have evolved. Entrainment to these cues allow organisms to rhythmically set the pace of their own endogenous biological clocks with which the timings of diverse cellular activities are coordinated. In recent years, our knowledge of biological rhythms has extended across all domains of life. This includes both free-living and symbiotic life forms. With the insurgence of metagenomic sequencing tools, the field of holobiont chronobiomics (encompassing chronobiology of host and its associated microbiota) has recently opened and gained significant traction. Here, we review current knowledge regarding free-living prokaryote rhythmic regulation before exploring active areas of research that consider the coordinated rhythmic regulatory activities of hosts and their symbionts as a single entity, i.e., holobiont, and even the extent to which rhythmicity influences virus–host interactions. We describe rhythmicity within non-photosynthetic bacteria, cyanobacteria, and archaea, before investigating the effect of light, and, thus, diel cycle, on viral life cycles and host–virus population dynamics in marine planktonic ecosystems along with their potential to influence host cyanobacterial circadian clocks. We then explore current evidence outlining coordinated rhythmic regulation within marine holobionts and the significance of this for holobiont health and adaptive fitness that, in turn, optimizes their success within their local environments. Finally, we assess the critical role of circadian regulation for holobiont innate immunity and metabolism within well-studied non-marine mammalian systems, and, thus, assess how this can guide us within understudied marine chronobiomics research.

Highlights

The phrase “no man is an island” as put by the 17th-century metaphysical poet John Donne in his prose work ‘Devotions upon Emergent Occasions’ talks about how humans do not do well in isolation and require a community to thrive (Donne, 1987)
We propose that future chronobiomics (Supplementary Box 1) research should increase its focus upon globally diverse and dominant phyla that comprise basal marine metazoa, such as Porifera, Cnidaria, and Ctenophora
The trophic interactions within large-scale planktonic systems, including the viral shunt, are extremely important for global biogeochemical cycling on a humungous scale, with numerous downstream effects for energy transfer within locally significant ecosystems, such as tropical coral reefs or deep-sea habitats. Dominant cues such as environmental light entrain the rhythms for free-living prokaryotes and viruses within large-scale planktonic communities

Summary

Introduction

The phrase “no man is an island” as put by the 17th-century metaphysical poet John Donne in his prose work ‘Devotions upon Emergent Occasions’ talks about how humans do not do well in isolation and require a community to thrive (Donne, 1987). In light of current research, it is becoming increasingly evident that no organism can be considered in isolation. Beyond considering organisms within the ecological communities they reside in, it is imperative we consider the ecological communities they harbor within— their microbiome. Since the dawn of metagenomic sequencing, research into microbiome community composition has exponentially advanced, shedding light on the complexity of host–symbiont relationships (Huttenhower et al, 2014; Norman et al, 2014; Yoon et al, 2015; Jovel et al, 2016). Rhythmic regulations, including the circadian (Supplementary Box 1) rhythms (∼24-h endogenous biological clocks; Supplementary Box 2) set a metronome for coordinated activity across all domains of life (Edgar et al, 2012), and warrant exploration of their critical role in mediating individual cellular activity and for their role in mediating the rhythmically coordinated activities between host and their symbionts, facilitating successful adaptive optimization of the holobiont (Supplementary Box 1)

Objectives

Findings

Conclusion