Causative Agents of Bacterial Mortality in Marine Ecosystems

Mortality of Microbes in Aquatic Environments

Microbial Biosystems: New Frontiers

Proceedings of the 8

International Symposium on Microbial Ecology

Bell CR, Brylinsky M, Johnson-Green P (eds)

Atlantic Canada Society for Microbial Ecology, Halifax, Canada, 1999.

Causative Agents of Bacterial Mortality and the Consequences

to Marine Food Webs

J.A. Fuhrman, R.T. Noble

Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-0371

ABSTRACT

It has been known for about 20 years that production of planktonic heterotrophic bacteria

represents a large fraction of the flow of energy and matter in aquatic systems. We also

know that prokaryotic photoautotrophs, including cyanobacteria and prochlorophytes, are

very important in global primary production. It is critically important to know the fates of

these organisms, specifically the causative agents of their mortality, in order to understand

the patterns of energy flows and nutrient cycles in such systems. Starvation as a cause of

mortality is functionally different from actual removal, because starved cells must still be

removed at a rate similar to the starvation rate, or they would accumulate and continue to

increase over time (not observed). A decade ago, it was generally believed that protists,

primarily small flagellates, were the only significant agents for the removal or disappearance

of bacteria. However, a broad variety of evidence accumulated over the past decade

suggests that viruses are also responsible for considerable amounts of microbial mortality,

apparently of a magnitude comparable to protist-based mortality. Viral infection leads to

cell lysis and release of the cell contents which then become available for subsequent

bacterial uptake. Thus, this mode of mortality leads to a closed loop that increases bacterial

production and respiration while regenerating inorganic nutrients. Models show that this

robs matter and energy from larger organisms and forces more of the “action” of the system

into the bacteria. Viruses may also exert a strong influence on plankton species

composition and lead to increased biodiversity, because viral infection is density-dependent

and largely species-specific. This mortality contrasts with that caused by protists, which

apparently can graze most any bacterium and can reduce even a highly diverse mixture of

bacteria to low levels. Other, less known, mortality mechanisms include antibiosis,

predatory bacteria, and aggregation followed by sinking.

Introduction

It is now clear that microbes are critical and quantitatively significant components of aquatic

food webs and have numerous roles [3, 8]. While much attention has focused on the

production of bacterial biomass, it is often more important to understand the fate of that

biomass, particularly the bacterial mortality. This brief review will summarize the various

causative agents and discuss what is known about their significance in planktonic systems.

Mortality of Microbes in Aquatic Environments

Possible Causative Agents of Mortality

Protist Grazing

This mechanism has been known for decades to be significant, and for many years it was

considered to be the primary cause of bacterial mortality [13]. Grazing on individual

bacteria is thought to be dominated by flagellates due to the small size of the prey, although

ciliates and some sarcodines also participate [13]. Grazing is thought to be relatively

indiscriminate in that protists can feed on diverse bacterial assemblages. Flagellates usually

intercept their prey by collision and capture it into a vacuole. Digestion within the vacuole

is relatively rapid and often completed in tens of minutes or less. Undigested material is

released in what is sometimes called ‘pico pellets’. Because flagellates have fast potential

growth rates (doubling a few times per day), they are capable of responding to varying

conditions and can grow fast enough to keep bacteria in check under most natural aquatic

conditions.

Viral Infection

Although known from pure cultures for several decades (reviewed by Fuhrman and Suttle

[10]) viruses of aquatic microbes have been considered quantitatively significant

components of aquatic systems for only about a decade [4, 17, 18]. Viruses are thought to

be specific for their hosts (usually species or strain), and are density-dependent because they

rely on diffusion to pass from host to host. Lytic infection results in bursting of the host cell

with release of the cell contents and progeny viruses. Whether this cell debris resembles

bacterial ‘ghosts’ or simply amorphous material is a matter of debate. Although the

existence of chronic infection is known, in which the progeny viruses are released

continuously (without bursting the host), its significance in nature is unknown. There is

evidence from marine systems of the common occurrence of lysogeny, in which a viral

genome is integrated into the host genome and reproduced with it over many generations

[12]. However, it appears that induction of the lytic cycle from lysogens is relatively rare

compared to successive lytic infection [23]. Viruses are capable of rapid proliferation and

can quickly decimate populations of susceptible bacteria, as is readily shown in pure culture.

Defenses against viruses may include extracellular proteases and nucleases, mutated or

missing cell surface receptors, intracellular restriction enzymes, genetic incompatibility, and

immunity via prophage [1]. Viruses may counter these defenses, and resistance may reduce

a cell’s growth rate, so bacteria and viruses may be thought of as being in a constant battle.

Interestingly, attempted viral infection of an immune bacterium may feed the bacterium.

Predatory Bacteria

Some bacteria attack and feed on other bacteria by a variety of mechanisms. Examples are

Bdellovibrio, Vampirococcus, Daptobacter

, and there are almost certainly many unknown

others. In natural aquatic systems, their significance is poorly known. The species range of

bacterial prey varies, depending on the predator. The remains of the prey are usually cell

debris, which is probably not usually recognizable as a cell.

Starvation

This mechanism is often discussed [15], but there are few data on its quantitative

significance in nature. Though many species in culture produce small cells upon starvation,

Mortality of Microbes in Aquatic Environments

it does not necessarily follow that all small bacteria are starved. The common ability of

bacteria to survive for long times upon starvation in some kind of semi-resting state [15]

suggests that mortality from this mechanism is probably rare. A starved cell, even if dead,

may be ordinary-looking by standard microscopy, and is still suitable (albeit low-calorie)

food for grazers, although small molecules would leak out and storage reserves would be

exhausted.

Antibiosis (“Microbe-wars”)

Antibiotics may come from other microbes, including protists, and higher eukaryotes. Their

significance in aquatic food webs is not known. Some are bacteriostatic, with a temporary

effect on growth, while others are bacteriocidal, and kill the target cell. Cells affected by

antibiotics may appear normal, or may be enlarged, elongated, distorted, or broken up.

Defenses against antibiotics include hydrolytic enzymes, mutated targets, and modified

transport systems.

Virus-Related Processes Not Leading to Viral Reproduction

There are a variety of mechanisms by which viruses or viral components may damage cells

without having the virus reproduce [7]. They are poorly understood, especially in natural

systems. Cells that fall victim may be intact or broken up. The range of target cells may be

wide or narrow.

Aggregation Followed by Sinking and Grazing

Aggregation of particles, including bacteria, is a common process in aquatic systems [2].

Such aggregates often sink, transporting material downward. Aggregates are large enough

to be grazed by metazoa, including fish.

Ecological and Biogeochemical Consequences

Protists

Grazing leads to trophic transfer, and due to inherent inefficiencies, there are significant

respiratory ‘losses’ (concomitant with nutrient regeneration). Such losses always occur in

food webs, so they are not particularly high for heterotrophic microbes (i.e., the protist-

bacteria part of the microbial loop is not necessarily a sink).

Viruses

As discussed extensively [5, 8, 17], the release of cell contents and progeny viruses can lead

to a semi-closed cycle of bacterial uptake and release of organic matter. The net result is to

oxidize organic matter (a sink) and release inorganic nutrients. Quantitative models show

the result of having 50% of bacteria mortality from viruses (compared to 0%) is to increase

the bacterial production and respiration rate by about one third, depriving energy from

higher trophic levels and regenerating nutrients [8]. Note that the bacteria, viruses, and

dissolved substances do not sink, so this process helps maintain nutrients (N, P, Fe, etc.)

higher up in the water column.

Recent experiments confirm that lysis products are available to bacteria [14, 16]. In a

series of experiments in California, native viral lysis products (viruses plus cell debris) were

digested rapidly, but the digested tritium-labeled macromolecules were accumulated slowly,

Overview

Causative Agents of Bacterial Mortality in Marine Ecosystems

Causative agents of bacterial mortality play a crucial role in marine food webs, influencing energy flow and nutrient cycling. This study by J.A. Fuhrman and R.T. Noble explores the significance of various mortality mechanisms, including protist grazing and viral infection, in aquatic environments. Understanding these processes is vital for marine ecologists and researchers studying microbial ecology. The document reviews evidence on how these agents affect bacterial populations and their broader ecological impacts, providing insights into the dynamics of marine ecosystems. It is essential for students and professionals interested in marine biology and microbial ecology. Key Points Explores the role of protist grazing in bacterial mortality in marine ecosystems. Discusses the impact …

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FAQs

What are the main causes of bacterial mortality in marine environments?

Bacterial mortality in marine environments is primarily caused by protist grazing and viral infections. Protists, particularly flagellates, consume bacteria rapidly, while viruses can lead to cell lysis, releasing nutrients back into the ecosystem. Other factors include predatory bacteria and antibiosis, where microbes produce substances that inhibit or kill other bacteria. Understanding these mechanisms is essential for grasping how energy and nutrients flow through marine food webs.

How do viruses influence bacterial populations in aquatic systems?

Viruses significantly influence bacterial populations through lytic infections, which result in the destruction of host cells and the release of organic matter. This process not only reduces bacterial numbers but also recycles nutrients, making them available for other organisms. Viral infections are often density-dependent, meaning they target more abundant bacterial species, which can lead to shifts in community composition and increased biodiversity. This dynamic interaction highlights the complex relationships within marine microbial ecosystems.

What is the significance of understanding bacterial mortality in marine food webs?

Understanding bacterial mortality is crucial for comprehending the functioning of marine food webs. Bacteria serve as primary producers and decomposers, playing a vital role in nutrient cycling and energy flow. By studying the factors that contribute to bacterial mortality, researchers can better understand how these processes affect higher trophic levels and overall ecosystem health. Insights gained can inform conservation efforts and management strategies in marine environments.

What methods are used to study bacterial mortality mechanisms?

Various methods are employed to study bacterial mortality mechanisms, including microscopy to observe infected cells, and tracer techniques using fluorescently labeled bacteria. Researchers also measure viral decay rates and viral production to estimate the impact of viruses on bacterial populations. These methodologies allow scientists to quantify the contributions of different mortality agents and understand their ecological implications in marine ecosystems.