Evolution in Brownian space a model for the origin of the bacterial flagellum N J Mtzke.pdf

Evolution in (Brownian) space: a model for the origin of the

bacterial flagellum

Version 1.0 (last updated November 10, 2003)

( Update section added September 2006.)

E-mail address: matzke@ATncseweb. (please remove obvious anti-spam modification)

Abstract: The bacterial flagellum is a complex molecular system with multiple

components required for functional motility. Such systems are sometimes proposed

as puzzles for evolutionary theory on the assumption that selection would have no

function to act on until all components are in place. Previous work (Thornhill and

Ussery, 2000, A classification of possible routes of Darwinian evolution. J Theor

Biol. 203 (2), 111-116) has outlined the general pathways by which Darwinian

mechanisms can produce multi-component systems. However, published attempts to

explain flagellar origins suffer from vagueness and are inconsistent with recent

discoveries and the constraints imposed by Brownian motion. A new model is

proposed based on two major arguments. First, analysis of dispersal at low

Reynolds numbers indicates that even very crude motility can be beneficial for large

bacteria. Second, homologies between flagellar and nonflagellar proteins suggest

ancestral systems with functions other than motility. The model consists of six

major stages: export apparatus, secretion system, adhesion system, pilus, undirected

motility, and taxis-enabled motility. The selectability of each stage is documented

using analogies with present-day systems. Conclusions include: (1) There is a strong

possibility, previously unrecognized, of further homologies between the type III

export apparatus and F 1 F 0 -ATP synthetase. (2) Much of the flagellum’s complexity

evolved after crude motility was in place, via internal gene duplications and

subfunctionalization. (3) Only one major system-level change of function, and four

minor shifts of function, need be invoked to explain the origin of the flagellum; this

involves five subsystem-level cooption events. (4) The transition between each stage

is bridgeable by the evolution of a single new binding site, coupling two pre-existing

subsystems, followed by coevolutionary optimization of components. Therefore, like

the eye contemplated by Darwin, careful analysis shows that there are no major

obstacles to gradual evolution of the flagellum.

Contents:

Update (September 2006)

• 1.1. A complex contrivance

• 1.2. An evolutionary puzzle

• Figure 1: Composite electron micrograph of the flagellum basal

body and hook

• 1.3. Theory: the evolution of systems with multiple required

components

• 1.4. Constructing and testing evolutionary models

• 2.1. Modern flagella

• Figure 2: Schematic diagram of a typical bacterial flagellum

• Table 1: Structural components of the

E. coli

flagellum

• Table 2: Components of the

E. coli

regulation/assembly and

chemotaxis systems

• 2.2. Previous attempts to explain flagellar origins

• 2.2.1. Short discussions

• Table 3: Some microbial motility systems

• 2.2.2. Cavalier-Smith (1987)

• 2.2.3. Rizzotti (2000)

• Figure 3: Rizzotti's (2000) scenario for the origin of a

proto-flagellum from an F 1 F 0 ATP synthetase

• 3.1. Phylogenetic context and assumed starting organism

• 3.2. Starting point: protein export system

• 3.2.1. Type III secretion systems

• Figure 4: Systems with components homologous to

flagellar components

• Figure 5: Various secretion systems of prokaryotes

• 3.2.2. Are nonflagellar type III secretion systems derived from

flagella?

• 3.2.3. An ancestral type III secretion system is plausible

• Table 4: Convergent functions of well-characterized

prokaryote secretion systems

• 3.2.4. The origin of a primitive type III export system

• 3.2.5. The relationship between type III export and the F

1 F 0 -

ATP synthetase

• Table 5: Similarities between proteins of the F

1 F 0 -ATP

synthetase and the flagellar type III export apparatus

that may suggest homology

• 3.3. Type III secretion system

• 3.4. Origin of a type III pilus

• 3.4.1. Filament-first hypothesis

• 3.4.3. Modified filament-first hypothesis

• 3.4.4. Improvements on the type III pilus

• 3.5. The evolution of flagella

• 3.5.1. The selective advantage of undirected motility

• Figure 6: Relative diffusion advantage of motility as a

1. Introduction

2. Background

3. The Model

• 3.4.2. Cap-first hypothesis

function of cell size and absolute swimming velocity

• 3.5.2. Primitive flagella

• 3.5.5. Chemotaxis and switching

• 3.5.6. Hook and additional axial components

• 3.5.7. Modern variations

4. Conclusions

• Figure 7: Summary of the evolutionary model for the origin of

the flagellum, showing the six major stages and key

intermediates

• 4.1. Evaluating the model

• Table 6: Functions and analogs at each stage of the presented

model

• 4.2. The evolution of other microbial motility systems

• 4.3. The construction of evolutionary models

5. Acknowledgements

6. References

Update, September 2006

This essay has now been cited in the literature (Pallen et al . 2006, “Evolutionary

links between FliH/YscL-like proteins from bacterial type III secretion systems and

second-stalk components of the FoF1 and vacuolar ATPases.” Protein Science , 15(4),

935-941 - DOI ) and linked from a peer-reviewed article I have just coauthored

(Pallen and Matzke 2006, “From The Origin of Species to the origin of bacterial

flagella.” Nature Reviews Microbiology , 4(10), 784-790. Advanced Online Publication

on September 5, 2006 - DOI ) . Therefore, in order to avoid confusion, I will not

update the text of this article at this address. I have, however, made some minor

formatting changes, and updated the Reader Background page .

While “Evolution in (Brownian) Space” was admittedly a first attempt, and I was a

dedicated enthusiast rather than a professional, I think the model has stood up

rather well over the last two and a half years. Writing in 2006, I would still agree

with about 90% of the 2003 model. To summarize the major updates I would make:

First, the hypothesis of homology between the Type 3 Secretion System export

apparatus and the F 1 F 0 -ATPase (and its archaeal and eukaryotic equivalents) has

been dramatically strengthened by the findings of two papers, Lane et al . 2006

(“Molecular basis of the interaction between the flagellar export proteins FliI and

FliH from Helicobacter pylori .” Journal of Biological Chemistry, 281(1), 508-17 -

DOI ) , and the aforementioned Pallen

et al

• 3.5.3. Loss of outer membrane secretin

• 3.5.4. Refinements

. As I predicted in 2003, sequence

studies have now confirmed homology between FliH/YscL and F 0 -b (and its

equivalents in other ATPases). They also strongly indicate that F 1 -delta is

homologous to the C-terminal domain of FliH; I did not predict this, but it does

. 2006

further confirm my more general prediction of “a strong possibility, previously

unrecognized, of further homologies between the type III export apparatus and

F 1 F 0 -ATP synthetase.” However, I would retract some of my more speculative

suggestions for ATPase homology to FliJ, FliO, and FliP (FliJ and FliO are

apparently not even universally required in flagella). I am still hopeful regarding

the suggestions for FliQ and FliR.

and various minor points now have me leaning

somewhat towards the view that the flagellar and nonflagellar systems are sister

groups, and the NF-T3SS is therefore an outgroup. However, as we note in Pallen

and Matzke 2006 the scientific community is split on this question. There are several

avenues of investigation that might clarify matters, which I will explore in the

future.

Thirdly, the question of which proteins are actually universally “essential” for

flagellum function, and which proteins have homology to other flagellar proteins or

nonflagellar proteins, has been systematically reviewed in Table 1 of Pallen and

Matzke (2006). I have reposted the table in my blog post on Panda's Thumb . It is

important to note that this table is much more conservative than the Matzke 2003

homology suggestions, which ranged from well-established to loose speculation. The

homologies in the 2006 table are all well-confirmed by standard BLAST techniques,

except for five proteins where homology is based on structural or other similarities.

Even for these five, two of the flagllar proteins have other known homologies based

on sequence (FliC to FlgL and FliH to YscL), two are not universally essential (FliH

and FliJ), and three of the homologies have been repeatedly put forward in the

literature (FliC to EspA, FliK to YscP, and FliH/YscL to F 0 -b+F 1 -delta and

equivalents). In the entire list, only one required protein has a new proposed

homology that could be considered speculative (FliG, to MgtE).

Many of the homologous and/or inessential proteins found in Table 1 of Pallen and

Matzke 2006 were cited in the 2003 paper, but the 2006 table is an authoritative

update and supercedes what is said here. The important overall point, as discussed

in my blog post , is that of the 42 proteins in Table 1 of Pallen and Matzke, only two

proteins, FliE and FlgD, are both essential and have no identified homologous

proteins. This is substantially more impressive than the situation in 2003, and means

that the evidence for the evolutionary origin of the flagellum by standard gene

duplication and cooption processes is even stronger than in 2003. Important specific

updates include: a homolog of FlgA has been confirmed (along the lines that I

suggested in 2003); FliG has no homolog in NF-T3SS or the Exb/Tol systems, rather

it may be homologous to the magnesium transporter MgtE; and the flagellar

filament protein FliC (and its sister FlgL) is probably homologous to EspA and

other pilus proteins found in NF-T3SS. I still suspect that all of the axial proteins

(including FliE and FlgD) are homologous to each other and therefore to pilus

proteins in NF-T3SS, but only the confirmed homologies are reported in Pallen and

Matzke 2006.

Secondly, in the 2003 essay I for the most part assumed that the nonflagellar Type 3

Secretion System (NF-T3SS) was derived from the flagellum, rather than being an

outgroup with a sister group relationship. I took this position partially to show that

even under this assumption the evidence for evolution was strong, and partially

because the evidence seemed to lean slightly in that direction. The parsimony

argument of Pallen

et al

. 2005

(“Type III secretion: what's in a name?” Trends in

Microbiology 14(4), 157-160, April 2006 - DOI ) . As they point out, the terminological

distinction between "flagellum" and "type 3 secretion system" is dubious and

artificial, and it is more true to acknowledge that flagella have a type III secretion

system. Therefore, there are two known groups of type III secretion systems,

flagellar and nonflagellar, abbreviated F-T3SS and NF-T3SS.

There is much more to be said about recent research and its implications for

flagellum evolution. For the near future I intend to post my thoughts on this in the

new flagellum evolution section of the Panda's Thumb blog.

1. Introduction

1.1. A complex contrivance

The bacterial flagellum is one of the most striking organelles found in biology. In

Escherichia coli the flagellum is about 10 μm long, but the helical filament is only 20

nm wide and the basal body about 45 nm wide. The flagellum is made up of

approximately 20 major protein parts with another 20-30 proteins with roles in

construction and taxis (Berg, 2003; Macnab, 2003). Many but not all of these

proteins are required for assembly and function, with modest variation between

species. Over several decades, thousands of papers have gradually elucidated the

structure, construction, and detailed workings of the flagellum. The conclusions

have often been surprising. Berg and Anderson (1973) made the first convincing

case that the flagellar filament was powered by a rotary motor. This hypothesis was

dramatically confirmed when flagellar filaments were attached to coverslips and the

rotation of cells was directly observed (Silverman and Simon, 1974). The energy

source for the motor is proton motive force rather than ATP (Manson et al. , 1977).

The flagellar filament is assembled from the inside out, with flagellin monomers

added at the distal tip after export through a hollow channel inside the flagellar

filament (Emerson et al. , 1970). The flagella of E. coli rotate bidirectionally at about

100 Hz, propelling the rod-shaped cell (dimensions 1x2 μm) 10-30 μm/sec. The

flagella of other species, powered by sodium ions rather than hydrogen ions, can

rotate at over 1500 Hz and move cells at speeds of several hundred μm/sec. The

efficiency of energy conversion from ion gradient to rotation may approach 100%

(DeRosier, 1998). The bacterial flagellum is now one of the best understood

molecular complexes, although numerous detailed questions remain concerning the

function of various protein components and the exact mechanism of torque

generation. However, the origins of this remarkable system have hardly been

examined. This article will propose a detailed model for the evolutionary origin of

the bacterial flagellum, along with an assessment of the available evidence and

proposal of further tests. That the time is ripe for a serious consideration of this

question is discussed below.

Finally, if I were doing a revision, I would update the terminology along the lines

suggested in Desvaux

et al

. 2006

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