Trends in Microbiology
OpinionBetween a Rock and a Soft Place: The Role of Viruses in Lithification of Modern Microbial Mats
Section snippets
‘Living Rocks’ – From Microbial Mat to Stromatolite
Stromatolites (see Glossary) (Figure 1) are lithified sedimentary biofilms constructed by microbial mat communities that represent the oldest ecosystems on the planet; they have persisted continuously, albeit at variable abundance, throughout the geological record up to the present day [1]. Microbial mats (Figure 1) are laminated organosedimentary ecosystems with a characteristic mesofabric that is reminiscent of stromatolites [2]. Stromatolites provide evidence for some of the earliest life on
Vast Viral Abundance Influencing Global Biogeochemical Cycles
Viruses represent the most numerous ‘biological entity’; they are on the edge of life, unable to replicate without a host. Viruses are the ‘dark energy’ of the planet, the unseen driver that, through viral lysis, selection, and genetic exchange has major impacts on biogeochemical cycling [23]. Viral genomes exist in all forms of nucleic acid, from double-stranded to single-stranded DNA or RNA. Viruses of bacteria and some archaea are referred to as bacteriophages (or phages). Viruses represent
Recent Developments in Technologies to Facilitate Viral Analyses
Metagenomics and metatransciptomics approaches, in which nucleic acids are sequenced directly from a variety of ecosystems, have resulted in a renaissance of viral discovery. Viruses lack conserved universal genes, such as those seen in bacteria and archaea (16S–23S rRNAs) or in eukaryotes (18S–28S rRNAs); hence, direct sequencing is the only way to analyze viruses effectively [25]. Greater than 75% of all viral proteins have no sequence similarity to known proteins [34]; however,
Viral Lifestyle: The Double-edged Sword
Viruses (in particular, bacteriophages) have unique infection lifestyles. In phages, these are classically termed the ‘lytic cycle’ (in which phage DNA is replicated via infectious virion particles) and the ‘lysogenic cycle’ (in which phage DNA replication occurs within a bacterium but without the generation of infectious virion particles) [43]. Viral and phage lifestyles are classified in four unique stages ranging from I to IV [44] (Figure 2).
Stage I. This represents a strictly lytic virus
Model for Viral Influence in Stromatolite Formation
The role and influence of viruses in ancient and early Earth ecosystems represent a further challenge in our understanding of this enigmatic group of biological entities. Such ecosystems include our earliest examples of complex microbial communities: ‘stromatolites’. Modern stromatolites (e.g., the archetypal versions found in Shark Bay, Australia, as well as those in the Bahamas and Pavilion Lake) present a proxy on how viruses may have transformed, manipulated, and diversified ancient
Indirect Viral Mechanisms in Stromatolite Formation: Viral Lysis/Resistance Cycle
The first indirect viral mechanism is via lysis. In viral lysis, cellular components (e.g., DNA, RNA, proteins) are released as well as bound cation (e.g., calcium) and bicarbonate [56,57]. This mechanism potentially increases photosynthesis by the release of extra nutrients (e.g., nitrogenous compounds, cations, micronutrients, and bicarbonate) that increase primary production in cyanobacterial mats, and the release of lysed cellular components may also increase biofilm strength and nucleation
Direct Viral Mechanisms in Stromatolite Formation: Viral Manipulation of Host Metabolism
Viruses can also change the functional repertoire of an organism by vAMGs which alter metabolic flow from one pathway over another. Some cyanophages (i.e., phages infecting cyanobacteria) shut off Calvin cycle dark reactions to shift towards pentose phosphate pathways that result in increased nucleic acid synthesis for phage replication [55]. This increases the fitness of virus and host, as virus-encoded photosystems increase primary production in cyanobacteria contributing to host growth and
Viruses through Geological Time: Role in Early Life Evolution?
In addition to their critical role in carbon and nitrogen cycling in marine systems, described earlier, pelagic viruses also affect the carbonate chemistry of the ocean [70] and their direct role in CaCO3 nucleation has been proposed [56]. Indirectly, virus-induced lysis in cultures of pelagic cyanobacteria increased the alkalinity of the medium and led to carbonate precipitation [57], corroborating our proposed viral contribution to lithification of mats. Furthermore, an unidentified viral
Concluding Remarks and Future Directions
In conclusion, viruses may be the missing interaction in the transition from ‘soft’ nonlithified microbial mat to ‘hard’ lithified stromatolites. We hypothesize that lifestyle is coupled to the transition from microbial mat to stromatolite, which is a proxy for stromatolite hardness, and that viruses impact microbial metabolism in microbial mats and stromatolites by different pathways. A role for viruses in stromatolite and microbial mat functioning has been suggested [63,66,76,77] but not
Acknowledgments
We acknowledge funding and support from National Science Foundation (Division of Ocean Sciences) grant 1561173 to P.T.V.
Glossary
- Bacteriophage (phage)
- a virus of bacteria or archaea.
- Biological entity
- an entity involved in biological processes (e.g., ecology and evolution); this definition allows the inclusion of viruses as well as self-replicating living organisms.
- Biosignatures
- measurements that allow assessment of biological life, usually in the context of geology.
- BREX
- bacteriophage exclusion; this is an antiviral system, identified in bacteria, that allows for resistance to phage infection. BREX allows phage adsorption; it
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