Predatory Bacterium Feasts on Soil Microbiome

July 17, 2023

Biocrust growing on edge of red sandstone cave.
Biocrust formed over red sandstone.
Source: Wikimedia Commons
Bacterial predators kill other microbes and consume them as nutritional resources. Although the initial invasion may appear harmless, bacterial predators gradually consume host macromolecules and utilize them as nutrients. Thus, the microbial prey is essentially eaten alive from the inside out in a process that actively kills the host microbe and can have significant impact on the structure and function of all sorts of microbial communities, including communities of organisms living at the soil surface (ie., biocrusts).

Biocrusts are produced from an intimate association between soil particles and differing proportions of dehydration-tolerant photosynthetic and heterotrophic organisms that live within or immediately on top of the soil, including bacteria, fungi, lichens, liverworts, mosses, eukaryotic algae and cyanobacteria. Biocrusts usually grow in environments with little vegetation, particularly in arid regions where plants struggle to endure. They fix a substantial amount of carbon and nitrogen in the soil and are responsible for almost 15% of the net primary productivity of the terrestrial ecosystem.

In a recently published Nature Communications article, scientists proposed the epithet ‘Candidatus Cyanoraptor togatus,’ as a new generic and specific name for an obligatory intracellular bacterium that preys upon cyanobacteria in biocrusts and thus exerts substantial effects on the ecosystem.

Because biocrusts are slow-forming microbial communities that can take years to recover from predatory outbreaks, and increased temperatures and reduced rainfall resulting from climate change can make it even more difficult for biocrusts to recuperate from such disturbances, it is important to understand how predators like Cyanoraptor target key members of this ecological niche.

How Does Cyanoraptor Influence the Ecology of Biocrusts?

Cyanoraptor is a gram-negative bacterium belonging to the family Chitinophagaceae in the phylum Bacteroidetes, and it represents a new subgroup of prokaryotic predators, as it has no known relatives among other predatory prokaryotes. Cyanoraptor can completely wipe out healthy biocrusts, hampering important ecological functions, such as resilience to soil erosion, alteration of soil surface temperature, moisture retention, photosynthesis and soil fertility—all of which are integral for supporting plants in arid regions. 

Cyanroaptor Prey

Vulnerable Cyanoraptor hosts are filamentous, non-heterocystous cyanobacteria, who are typical pioneer biocrust formers. In the aforementioned study, researchers examined the effect of Cyanoraptor on diverse cyanobacterial strains and reported that out of 70 cyanobacterial strains that were tested in 14 genera, only 14 strains in 4 genera were susceptible to attack. Susceptible cyanobacterial species were all determined to be motile and included Microcoleus vaginatus, Allocoleopsis sp., Potamolinea sp. and Xeronema sp.

Microscopy of Cyanoraptor propagules entering cyanobacteria cell, then entering pseudo-filamentous stage and consuming host cells.
Microscopic view of various stages of Cyanoraptor's life cycle.
Source: Bethany et al./Nature Communications, Aug. 2022

Using meta-analyses, researchers were able to detect worldwide distribution of Cyanoraptor in biocrusts and observe prevalence of the predator in the southwest United States. However, additional data (via visualization of plaque surveys and 16S rRNA gene sequencing) are needed to verify these observations. Studying the prevalence and behavior of Cyanoraptor in understudied locations will be an important piece of this microbiological puzzle.

How Does Cyanoraptor Attack?

Cyanoraptor has an extracellular attack stage, but unlike any other known predatory prokaryote, Cyanoraptor is non-motile at all phases of its life (i.e., the organism lacks visible flagella and motility genes). Thus, Cyanoraptor behaves as an ambush predator, relying on the motility of its prey for survival. Cyanoraptor initiates infection by contact/docking with the host cell, effectively "hitchhiking" with the motile cyanobacteria. 

Predatory cells then enter the cyanobacterial cytoplasm to complete intracellular cell division. Cyanoraptor propagules (round units that transmit the pathogen) have an outer compartment, which is where scientists believe the predator stores its weapon—hydrolytic enzymes to target their prey. In fact, 3% of Cyanoraptor’s genes are hydrolytic enzymes with signal peptides that aid in secretion once inside host cells.

Intracellular Cyanoraptor have no outer compartments. After the bacterium enters a host cell, its outer compartment fuses with the cyanobacterial membrane, causing Cyanoraptor to assume a rod-like morphology and eventually grow into pseudo-filaments. The reason why Cyanoraptor adopts this particular morphology during its intracellular stage is still unknown. 

While the extracellular propagules do not divide, intracellular Cyanoraptor undergoes multiple cell divisions in the late pseudo-filamentous phase. However, Cyanoraptor possess only 2 biosynthesis pathways—glutamine and asparagine—making it dependent on its hosts for nutritional requirements. As Cyanoraptor grows and divides, it depletes the nutritional reserves of its host and builds a fibrillar covering called a cocoon.

In the late intracellular phase, extracellular vesicles are again produced in the area between the cell and its newly formed cocoon. These extracellular vesicles merge with the fibrillar cocoon and fuse around single Cyanoraptor cells to re-form the outer compartment that was lost when Cyanoraptor entered its cyanobacterial host. With its outer compartments restored, Cyanoraptor is ready to be released as infectious propagules from the host cell after degrading the cyanobacteria. All in all, by feasting on healthy cyanobacterial filaments, Cyanoraptor turns its host into carcass-like ghost filaments.
Simplified diagram showing the infection process of Cyanoraptor.
Simplified diagram showing the infection process of Cyanoraptor.
Source: Monolina Sarkar

What are the Consequences of Cyanoraptor Predation?

As Cyanoraptor consumes cyanobacteria in the soil, it leaves behind a clear area (plaque) on the lawn of the biocrust. Such decreases in microbial biomass also decrease organic carbon and nitrogen production, leading to imbalances in nutrient availability. Concentration of extracellular polysaccharide (EPS)—natural polymers secreted by microbes—also diminish, affecting critical functional features of biocrusts, including moisture retention and dust trapping capacity. Finally, as Cyanoraptor feasts, it helps make cyanobacterial biomass accessible to other adventitious bacteria, further altering microbiome population dynamics in the biocrust.

Biocrust reinstatement is aided by inoculating the soil surface with biocrust inoculum. However, biocrust restoration practices that rely on employing whole communities to produce said inoculum also pose the risk of further spreading the predator. Testing for diagnostic plaques in the initial inoculum and eliminating any diseased plaques can effectively avoid disease transmission between diseased and unaffected regions. In the long term, it is essential to study the dynamics of Cyanoraptor and its prey in order to understand and protect biocrust-dominated ecosystems from the effects of this functional damage.
Learn more about the role of microbes in climate change by browsing our climate change resources.

Author: Monolina Sarkar, M.S.,Ph.D.

Monolina Sarkar, M.S.,Ph.D.
Monolina Sarkar is a professor in the department of botany at Sammilani Mahavidyalaya, University of Calcutta.